Human Social Evolution

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Human Social Evolution
THE FOUNDATIONAL WORKS OF
RICHARD D. ALEXANDER

Edited by Kyle Summers

and
Bernard Crespi

1
3
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Library of Congress Cataloging-in-Publication Data

Human social evolution : the foundational works of Richard D. Alexander / edited by Kyle
Summers and Bernard Crespi.
pages cm
Includes bibliographical references.
ISBN 978–0–19–979175–0 (alk. paper)
1. Alexander, Richard D.—Influence. 2. Alexander, Richard D. —Criticism and
interpretation. 3. Human evolution. 4. Social evolution. 5. Natural selection.
I. Summers, Kyle.
GN281.H8495 2013
599.93’8—dc23
2013017153

9 8 7 6 5 4 3 2 1
Printed in the United States of America
on acid-free paper
CONTENTS

Contributors ix

Preface xi

Introduction – Kyle Summers and Bernard Crespi 1

PART I } General Foundations

1. Insect Behavior and Social Evolution 21
Introduction: From Cricket Taxonomy to a Darwinian Philosophy of
Man by Mary Jane West-Eberhard, Smithsonian Tropical Research
Institute 23
Excerpt from Alexander, R. D. 1969. Comparative animal behavior
and systematics. In: Systematic Biology. Proceedings of the International
Conference on Systematics (Ann Arbor, Michigan, July 1967). National
Academy of Sciences Publication 1962: 494–517. 29
2. Cooperation 39
Introduction: A New Theory of Cooperation by Steven Frank, University of
California at Irvine 40
Excerpt from: Alexander, R.D. 1986. The Biology of Moral Systems. New
York: Aldine Press. 48
3. Eusociality in Naked Mole-Rats 53
Introduction: Richard Alexander, the Naked Mole-Rat, and the Evolution
of Eusociality by Paul Sherman, Cornell University 55
Excerpt from Alexander, R.D., Noonan, K.M. and Crespi, B.J. 1991. The
Evolution of Eusociality. In P. Sherman, J. Jarvis and R.D. Alexander
(eds.). The Biology of the Naked Mole-Rat: 3–44. Princeton, NJ: Princeton
University Press. 63
4. Parent-Offspring Conflict and Manipulation 70
Introduction: The Evolution of Social Behavior by David Queller,
Washington University 71
Excerpt from Alexander, R.D. 1974. The evolution of social behavior.
Annual Review of Ecology and Systematics 5:325–383. 77
vi { Contents

PART II } Human Social Evolution

5. Biology and Culture 93
Introduction by Mark Flinn, University of Missouri 95
Excerpt from Alexander, R.D. Evolution and culture. In Evolutionary
Biology and Human Social Behavior: an Anthropological Perspective.
N. Chagnon and W.G. Irons (eds.): pp. 59–78. North Scituate, MA:
Duxbury Press. 104

6. Intergroup Competition and Within-group Cooperation 123

Introduction: Thinking about Human Aggression, Past and Present:
Alexander and Tinkle’s (1968) Review of Lorenz and Ardrey by Bobbi Low,
University of Michigan 125
Excerpt from Alexander, R.D. and Tinkle, D.W. 1968. Review of On
Aggression by Konrad Lorenz and The Territorial Imperative by Robert
Ardrey. Bioscience 18:245–248. 130

7. Kinship, Parental Care, and Human Societies 138

Introduction: Concealed Ovulation in Humans: Further Evidence by
Beverly Strassmann, University of Michigan 139
Excerpt from Alexander, R.D. and Noonan, K.M. 1979. Concealment of
ovulation, parental care, and human social evolution. In N.A. Chagnon
and W.G. Irons (eds.). Evolutionary Biology and Human Social Behavior:
An Anthropological Perspective. 436–453. North Scituate, MA: Duxbury
Press. 152
8. Human Childhood 171
Introduction: Altriciality, Neoteny, and Pleiotropy by Paul Turke,
University of Michigan 173
Altriciality: Why are human babies helpless? In Alexander, R.D. 1990. How
Did Humans Evolve? Reflections on a Uniquely Unique Species. University
of Michigan Museum of Zoology Special Publication 1:1–38. 182
9. Indirect Reciprocity 197
Introduction: The Basis of Morality, Richard Alexander on Indirect
Reciprocity by Karl Sigmund, University of Vienna 199
Excerpt from Alexander, R.D. 1986. The Biology of Moral Systems. New
York: Aldine Press. 209
10. The Evolution of Intelligence 232
Introduction: Reflections on the Evolution of the Human Psyche by R.I.M.
Dunbar, Oxford University 235
 Contents } vii

Alexander, R.D. Evolution of the Human Psyche 1989. In P. Mellars and

C. Stringer (eds.). The Human Revolution. Behavioral and Biological
Perspectives on the Origins of Modern Humans: pp. 455–513. Princeton, NJ:
Princeton University Press. 244
11. Evolution of Morality 305
Introduction: Twelve (More) Things about the Evolution of Morality that
Make People Nauseous by David Lahti, City University of New York 307
Alexander, R.D. Biology and the Moral Paradoxes. Journal of Biological
Structures 5:389–395. 325
12. Evolution and Humor 334
Introduction: The Adaptive Significance of Humor by Stan Braude,
Washington University 337
Alexander, R.D. Ostracism and Indirect Reciprocity: The Reproductive
Significance of Humor. 1986. Ethology and Sociobiology 7:253–270. 345
13. Ecological Constraints and Human Cooperation 364
Introduction: Darwin’s Question: How Can Sterility Evolve? by Laura
Betzig, The Adaptationist Program 365
Excerpt from Alexander, R.D., Noonan, K.M. and Crespi, B.J. 1991. The
Evolution of Eusociality. In P. Sherman, J. Jarvis and R.D. Alexander (eds.).
The Biology of the Naked Mole-Rat: pp. 3–44. Princeton, NJ: Princeton
University Press. 375
14. Evolution and Religion 379
Introduction: The Concept of God as a Metaphor for Social Unity: Richard
Alexander’s Hypothesis by William Irons, Northwestern University 381
Religion, Evolution and the Quest for Global Harmony–Original essay for
this volume 384
15. Evolution and the Arts 426
Introduction: Cornerstone to Capstone: Richard Alexander on Social
Selection and the Arts by Kyle Summers, East Carolina University &
Bernard Crespi, Simon Fraser University 429
Excerpt from Alexander, R.D. 2003. Evolutionary Selection and the Nature
of Humanity. Chapter 15. In: V. Hosle and Ch. Illies (eds.). Darwinism and
Philosophy. South Bend, IN: University of Notre Dame Press. 440

Index 453
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CONTRIBUTORS

Laura Betzig William Irons

The Adaptationist Program Department of Anthropology
Ann Arbor, MI, 48109 USA Northwestern University
[email protected] 1810 Hinman Avenue
Evanston, IL 60208-1310 USA
Stan Braude
[email protected]
Department of Biology
Washington University in St. Louis David C. Lahti
Campus Box 1137, One Brookings Drive Department of Biology
St. Louis, MO 63130-4899 USA Queens College, City University of
[email protected] New York
Bernard J. Crespi 65-30 Kissena Boulevard
Department of Biological Sciences Flushing, NY 11367 USA
Simon Fraser University [email protected]
8888 University Drive Bobbi Low
Burnaby, B.C. Canada V5A 1S6 School of Natural Resources and
[email protected] Environment
Robin I.M. Dunbar University of Michigan
Department of Psychology Ann Arbor, MI 48109 USA
Magdalen College [email protected]
University of Oxford David Queller
Oxford, OX1 2JD, United Kingdom Department of Biology
[email protected] Washington University in St. Louis
Mark Flinn Campus Box 1137, One Brookings Drive
Department of Anthropology St. Louis, MO 63130-4899 USA
University of Missouri [email protected]
Columbia, Missouri 65211-1440 USA Paul W. Sherman
[email protected] Department of Neurobiology and
Steven A. Frank Behavior
Department of Ecology and W307 Seeley G. Mudd Hall
Evolutionary Biology Cornell University
University of California Ithaca, NY, 14853 USA
Irvine, CA 92697-2525 USA [email protected]
[email protected]
x { Contributors

Karl Sigmund Paul Turke

Faculty for Mathematics Department of Pediatrics and
University of Vienna Communicable Diseases
Nordbergstrasse 15 University of Michigan
A-1090, Vienna, Austria Ann Arbor, MI 48109 USA
[email protected] [email protected]
Beverly I. Strassmann Mary Jane West-Eberhard
Department of Anthropology Smithsonian Tropical Research
University of Michigan Institute
419 West Hall, Apartado Postal 0843-03092
1085 S. University Ave. Panamá, República de Panamá
Ann Arbor, MI 48109-1107 USA [email protected]
[email protected]
Kyle Summers
Department of Biology
East Carolina University
Greenville, NC 27858 USA
[email protected]
PREFACE

This book is a tribute to one of the great minds in evolutionary biology, Richard
D. Alexander. His help and encouragement during our graduate careers at the
University of Michigan was invaluable to both of us, and we miss the penetrating
discussions of complex topics in human and animal behavior and evolution that
he loved to engage in. His contributions to science, and the humanities, should
become standard reading for generations to come, and we hope this volume will
help to make that goal a reality. Dr. Alexander provided unstinting help with vari-
ous facets of the process of developing and producing this volume, and we thank
him for his efforts.
We also would like to take this opportunity to thank all of the people who
contributed to this volume—their contributions have served to highlight Dr.
Alexander’s work, and illuminate the many contributions he has made to our
understanding of human social evolution. These contributors also illustrate how
Dr. Alexander’s legacy is being passed on through the scientists that he trained and
influenced during the course of his career. He taught so many of us how to think
about evolution, and humanity, and how to turn these thoughts into productive
science.
We also thank our families, who have tolerated our absent-mindedness, and
absences during the long hours and late nights required to complete this volume.
K.S. and B.C.
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Human Social Evolution
This page intentionally left blank
 Introduction
Kyle Summers and Bernard J. Crespi

After decades rife with science strife

It seems appropriate to join
The slice of life that plies the knife
Along the flip side of the coin
R. D. Alexander, 2011

Richard D. Alexander is a farmer and rancher, horse trainer, poet, story teller,
folk singer, song writer, musician, author, and a philosopher, as well as a husband
(to Lorrie Alexander), a parent, and a grandparent. He and his wife have run a
large farm in Manchester, Michigan for more than thirty-five years. Alexander
grew up in rural Illinois, the child of two school teachers turned livestock farmers.
His childhood passed without many of the conveniences of modern life, such as
electricity and indoor plumbing. His mother cooked on a wood stove, and light
after dark came from kerosene lamps. His family raised cows, pigs, and chickens
on feed they grew themselves, selling meat, eggs, and cream. Alexander grew up
doing “chores” that most people would consider hard labor, such as working his
own threshing team of draft horses on different farms across the county. He went
to school in a one room country schoolhouse with a single teacher for all grades.
In 1946, Alexander attended Blackburn College, where he was consigned to a sin-
gle dormitory with a mix of new high school graduates and veterans of World War
II who were returning to school. In high school, Alexander had no thought of
attending college, and when he first went to college he had no thought of a career
in academia. From these rural origins sprang an intellect that has transformed our
understanding of human social behavior and evolution and, we propose, ourselves.
Alexander’s intellectual curiosity about human evolution probably sprang from
his early experiences in church, where he found himself fascinated by the ques-
tions raised concerning human nature, yet dissatisfied by the answers proferred.
Early in his college career, during his time at Blackburn College, he realized that in
academia he could pursue any questions he thought were of interest. Although he
pursued coursework in philosophy at Illinois Normal University after transferring
from Blackburn, Alexander was struck by the lack of a model of human nature,
and ultimately turned to biology to pursue his interests. Before entering graduate
2 { Introduction

school, he did not have the opportunity to take a course in evolutionary biology,
and even after deciding to pursue graduate study in biology at the University of
Ohio, where he studied entomology (see ch. 1), there were few courses in evolu-
tionary biology available. Nevertheless, over time his interests in evolution crystal-
lized and motivated Alexander to pursue three of the most difficult and important
questions in biology: how the diversity of life came into being through the process
of speciation, how natural selection has shaped the complexity of life (including
our own minds), and the meaning of the extreme social attributes of humans (e.g.,
art, music, dance, religion) from an evolutionary perspective. Alexander was able
to pursue groundbreaking research on the first two questions as a graduate student
working on singing insects, but it was only after he had become a faculty member
at the University of Michigan that he began to focus on sociality, and particularly
on human social behavior.
Over a long career at the University of Michigan, Alexander became, we
would argue, the world’s leading thinker on human social behavior from an evo-
lutionary perspective. His publications on this topic trace back to a remarkable
review in 1968 (with Donald Tinkle) of two books (On Aggression by Konrad
Lorenz and The Territorial Imperative by Robert Ardrey), where he laid out a
hypothesis concerning the influence of intergroup competition on human social
behavior that continues to be influential today. It was obvious from this review
that Alexander had been thinking about these issues for a long time, and from
these beginnings sprang a long series of publications on human social evolution
that have continued throughout his career at the University of Michigan, and
beyond.
A key watershed occurred with the publication of Alexander’s first book on
human social evolution: Darwinism and Human Affairs, in 1979 (The University
of Washington Press). In developing his ideas for this book, Alexander was greatly
influenced by the profound insights of three contemporaries: George Williams,
who taught biologists how to think about selection at the level of individual
rather than species benefit, William Hamilton, whose inclusive fitness theory, and
evolutionary stable strategy reasoning, taught us how to apply selection think-
ing at the levels of genes, families, and evolving traits, and Robert Trivers, who
first explained how kin cooperation and kin conflict are necessarily enmixed, and
how reciprocity can evolve, especially in species with powerful cognitive abilities,
such as humans. This was a time of Darwinian revolution for the study of behav-
ior, when the conceptual tools for understanding behavioral phenotypes, espe-
cially conflicts and confluences of interest, first came together. In Darwinism and
Human Affairs, Alexander first applied many of the key theoretical approaches
that these three researchers had developed—and many of his own—to human
social behavior in a comprehensive and systematic way, providing the most com-
plete and rigorous overview of the entire scope of human social behavior from an
evolutionary perspective achieved to that point.
 Introduction } 3

After the publication of Darwinism and Human Affairs, a veritable flood of

research on human social behavior was initiated by evolution-minded scientists,
not only in biology but in many other fields. The major themes that Alexander laid
out in his first book continue to be the focus of intense interest and debate in the
study of human social behavior today, including kinship and nepotism, direct and
indirect reciprocity, ontogeny, life history and senescence, the evolution of culture,
deceit and self-deception, innate and learned behavior, morality, law and justice,
and the evolution of artistic expression, among others.
Many years have passed since Darwinism and Human Affairs, and in this time
Alexander, his students and colleagues, and many others, have been construct-
ing a new evolutionary synthesis upon these themes, a synthesis that has grown
to encompass anthropology, psychology, psychiatry, economics, sociology, the
arts, humanities, and religion. This volume is a celebration of Richard Alexander’s
work, and his diverse, enduring influences in the study of virtually all aspects of
humanity. For each chapter we have chosen an excerpt from a key paper or chapter
that represents a particular theme that Alexander wrote about over the course of
his career. Each chapter is introduced by an expert in the field, most of whom are
former students or colleagues of Dr. Alexander, who provides perspective on how
his ideas have advanced scientific thought.
We believe this structure for the book is appropriate because Alexander con-
stantly strove to inspire his students and colleagues to think carefully about evolu-
tion and human behavior, and to develop and test novel, integrative hypotheses.
In his classic “Evolution and Human Behavior” course, taught for decades at the
University of Michigan, Alexander would challenge any and all students (under-
graduate and graduate) to try and find errors in his arguments, and to develop
their own alternative hypotheses. Alexander would carefully read hundreds of
essays, and provide firm yet helpful comments to all the students in this very pop-
ular (and hence very large) class. That some of his students took him up on this
challenge is apparent from this volume. Beverly Strassmann, for instance, wrote
a paper in this class as an undergraduate that has itself become a classic in the
field of human social evolution (Strassmann 1981). But this is just a start—all of
the students and colleagues of Alexander who have written introductory essays
for this volume have gone on to develop their own research programs in social
evolution, and those authors who did not directly interact with Alexander were
nonetheless inspired by his published work as they developed their own theories.
Even the essays themselves reveal the profound influence of Alexander’s philoso-
phy. For example, Paul Turke, in his essay, proposes a novel hypothesis connecting
altriciality and neoteny to the delayed senescence that characterizes the human
species relative to other primates. Even in the short space of an introduction,
Alexander’s associates cannot help but explore novel connections and new ideas.
This is a major part of Alexander’s legacy—a cadre of evolutionary thinkers who,
inspired by his example, have spent their lives developing and testing hypotheses
4 { Introduction

concerning social evolution, and especially the social evolution of that most com-
plicated of species, ourselves.

One

Chapter 1 by one of Alexander’s first graduate students, Mary Jane West-Eberhard,

provides an overview of Alexander’s early work on communication and mating
behavior. West-Eberhard is a staff scientist at the Smithsonian Tropical Research
Institute. She is one of the world’s leading experts on the behavior and evolution of
social wasps, and has also published on sexual and social selection in general, and
in relation to speciation, as well as a groundbreaking body of theory connecting
developmental mechanisms to evolutionary phenomena, including morphologi-
cal and behavioral change under selection, and population divergence and specia-
tion. The chapter provides a brief synopsis of some of Alexander’s early work on
communication, mating behavior, and speciation in insects, and some of his early
thoughts on human evolution. West-Eberhard shows how one of his papers was
a bridge between his earlier writings and the later ones on human evolution. She
argues that Alexander’s exceptional abilities to illuminate the evolutionary basis
of human social behavior stemmed from his strong background in the systemat-
ics and evolutionary biology of the singing insects, and his pioneering work on
Darwinian approaches to behavior in nonhuman animals.

Two

In chapter 2, Steven Frank explores a new view of the evolution of cooperation that
was developed by Alexander, as illustrated by an excerpt from his second book on
human social evolution, The Biology of Moral Systems (1987). Frank, a professor of
evolutionary biology at the University of California at Irvine, is one of the world’s
leading evolutionary theoreticians. His work has transformed our understanding
of inclusive fitness, multilevel selection, sex ratio evolution, parasite-host coevolu-
tion, and genetic conflict, among many other topics. Frank began his pursuit of a
career in evolutionary biology after taking Alexander’s class in animal behavior
as an undergraduate. He was a graduate student of the late William Hamilton,
but was also advised by Alexander. He points out that the extensive cooperative
networks that are part and parcel of the vast nation-states that characterize human
society are not easily explained by the twin pillars of cooperation developed in
evolutionary biology: kinship and reciprocity. He argues that Alexander’s work
led to a new view of how these cooperative networks could evolve and remain
stable: group suppression of conflict. Alexander’s ideas in this vein followed from
two parallel themes that he pursued over the course of his career: the evolution
of morality and justice, and the evolution of individuals at different levels in the
 Introduction } 5

hierarchy of life over the course of evolution. These ideas were stimulated by the
work of other great thinkers (such as John Rawls in the case of morality, and
Egbert Leigh in the case of conflict suppression in the evolution of the hierar-
chy of life), yet he developed a unique synthesis that made the generality of the
concepts clear. The theoretical underpinnings of this mechanism have now been
developed and refined (by Steven Frank and others), and it has become another
general principle upon which our understanding of the evolution of cooperation
rests. The idea has far-reaching implications. For example, as Alexander stresses in
the Biology of Moral Systems, the reproductive opportunity-leveling characteristic
of large democratic nation-states may have led to their notable success at warfare
and territorial expansion at the expense of more despotic regimes. In fact, the col-
lapse of despotism (which was the rule rather than the exception during the long
course of human history following the development of agriculture) may well have
been driven by this dynamic. After all, the prospect of fighting and risking one’s
life for king and country is less appealing when the royal elite have monopolized
most of the women.

Three

In chapter three, Paul Sherman introduces an excerpt from a classic paper on the
evolution of eusociality (by Alexander, Noonan, and Crespi), published in 1991 in
an edited volume entitled The Biology of the Naked Mole-Rat. Sherman, a profes-
sor of biology at Cornell University, is a world-renowned researcher in the field of
animal behavior, having carried out groundbreaking studies on the social behavior
of ground squirrels, naked mole rats, and wood ducks, among other organisms. He
is also a leader in the field of evolutionary medicine, publishing innovative studies
of spices as antimicrobial agents, allergies as anticancer mechanisms, and morning
sickness as a toxin-avoidance mechanism, among many other topics. Sherman was
a graduate student of Alexander, and they later worked together to establish the
first naked mole-rat colonies in the United States, at the University of Michigan
and at Cornell University. Sherman relates the story of how Alexander conceived
of the key characteristics of a eusocial vertebrate as a thought experiment and pre-
diction before anyone was aware of the existence of such an animal. Remarkably,
Alexander’s description almost perfectly described the naked mole-rat, which was
the subject of research by the biologist Jennifer Jarvis in South Africa. The discov-
ery of a eusocial vertebrate allowed profound insights into the ecological and evo-
lutionary mechanisms that drove the evolution of eusociality, and in turn this led to
a flood of research and publications, culminating in The Biology of the Naked Mole-
Rat. Sherman points out that Alexander had been thinking about the evolution
of eusociality for a long time before writing the chapter, beginning with a strong
interest in the phenomenon as an entomologist studying social behavior. He notes
that Alexander et al. (1991) made several key points with respect to the evolution
6 { Introduction

of eusociality: First, the haplo-diploid system that characterizes the major eusocial
insect groups (ants, bees, and wasps) is not a sufficient explanation for the evolu-
tion of eusociality; second, eusociality is a much more general phenomenon than
initially appreciated, evolving convergently across vast spans of the tree of life;
and third, both intrinsic (genetic and developmental) and extrinsic (ecological)
factors must have been crucial for the evolution of eusociality. Alexander et al.
(1991) argued that both “ecological constraints” (environmentally imposed con-
straints on the ability of individuals to breed on their own) in the form of the need
for nest site protection from predation (an extrinsic factor), and levels of genetic
relatedness (kinship, an intrinsic factor), are crucial for the evolution of eusocial-
ity. Sherman emphasizes that the arguments presented in Alexander et al. (1991)
have become widely accepted, and the chapter has become an indispensible guide
to understanding the evolution of eusociality.

Four

Chapter 4, by David Queller, introduces an article that represents Alexander’s

(1974) first exposition of general theory for the evolution of social behavior across
all animals, including humans. Queller was a doctoral student with Alexander,
and has since gone on to become one of the foremost researchers working on
social evolution, in organisms from plants to wasps to slime molds to humans.
He describes how Alexander’s (1974) paper, integrating nepotism, reciprocity, and
his new idea—parental manipulation—served as a nexus for future theory and
research, which included extensions, inspiration, presages of much-later develop-
ments such as skew theory, and ultimately constructive assaults. Alexander (1974)
also marks his transition from mainly studying crickets, to mainly focusing on the
evolution of sociality, and his effective combining of studies of specific taxa and
big questions in social evolution is mirrored in the work of many of his students.

Five

The fifth chapter, by Mark Flinn, expands on a paper elucidating Alexander’s con-
ception of how culture, long a bastion defended against biology, evolves in the
contexts of the human psyche, human conflicts and confluences of interest, and
human beliefs concerning how best to respond to particular social and mate-
rial contingencies. As an evolutionary anthropologist who has also survived, and
prospered, in the biology-versus-culture debate that was catalyzed by the changes
in evolutionary theory that Alexander, Hamilton, Trivers, Williams, and others
developed, Flinn is uniquely suited to describe how Alexander provides a novel
behaviorally based perspective on human culture. Alexander’s analysis opened the
door for future researchers to study culture from the perspective of evolution-
ary biology. Flinn was one of the first through this door. He was influenced by
 Introduction } 7

Alexander beginning in high school, then as an undergraduate, Master’s student,

and Postdoctoral Fellow at the University of Michigan. They have co-authored two
papers on cultural evolution (Flinn & Alexander 1982, 2007). Flinn has developed
a research program that integrates cultural with biological anthropology—help-
ing to generate the recent, now-maturing field of evolutionary anthropology. He
is currently president–elect of an organization that Alexander helped create, the
Human Behavior & Evolution Society.

Six

In chapter 6, Bobbi Low introduces a 1968 review, written by Alexander and Tinkle,
for the journal Bioscience, of two books (On Aggression by Konrad Lorenz and The
Territorial Imperative by Robert Ardrey). Low is a professor of resource ecology in the
School of Natural Resources and the Environment, and a faculty associate in popula-
tion studies at the Institute for Social Research, both at the University of Michigan.
As a long-time colleague of Alexander, she was strongly influenced by his work.
Although she began her career studying life history evolution in nonhuman animals,
Low later developed a strong interest in human social evolution, and has contributed
seminal research to this field. For example, her work on the evolutionary ecology of
human mating strategies and family relationships is widely cited, comprising a clas-
sic body of work. She was also a pioneer in the use of long-term, extensive historical
demographic datasets from Scandanavian parish records to test predictions from
evolutionary theory relevant to human behavior and life history (Low quips that her
research concerns the “sex lives of dead Swedes”). As Low points out, Alexander and
Tinkle (1968) was no run-of-the-mill book review, but rather presented a novel case
for the importance of intergroup competition in driving the evolution of human
cognition and behavior. She provides crucial context for the review, which was pre-
sented long before the current surge of interest in the relationship between warfare
and human social evolution. Low also notes that Alexander and Tinkle developed
the hypothesis that intergroup competition was focused on access to resources, and
in particular, reproductive resources, long before behavioral ecologists began apply-
ing this sort of cost/benefit thinking to human behavior in any systematic way. Low
also highlights the sad fact that public attitudes toward evolutionary explanations of
human behavior (or anything else for that matter) have barely changed in the long
span of time that has passed since the review was published. Low’s introduction is
indeed a potent reminder of the importance of bringing these issues to the attention
of the public, even (or especially) now.

Seven

Chapter 7 reprints a classic paper on parental care and concealed ovulation by

Alexander and Noonan, published in 1979. This paper is introduced by Beverly
8 { Introduction

Strassmann, a professor in the Department of Anthropology at the University

of Michigan. Strassmann was a graduate student under Alexander’s supervision,
but was inspired by his ideas even before entering graduate school. In fact, while
taking Alexander’s “Evolution and Human Behavior” course at the University of
Michigan as an undergraduate, she wrote a term paper extending Alexander and
Noonan’s 1979 argument, emphasizing the benefits of concealed ovulation for sub-
ordinate males. This paper (Strassmann 1981) has itself gone on to become a classic
reference in the field. Strassmann notes that Alexander and Noonan’s emphasis on
the intimate connections between increased levels of intergroup competition, the
complexity of social interactions within groups, and the importance of increased
paternal care was novel and prescient, leading to a flood of new insights concern-
ing human social evolution. She points out that connecting the evolution of con-
cealed ovulation to the evolution of increased paternal care was an inspired and
pivotal contribution, clarifying causal connections that before then had been com-
pletely obscure. Strassmann’s paper further clarified these connections by showing
that it was particularly subordinate males that were most likely to benefit from
concealed ovulation, which promoted a male reproductive strategy that empha-
sized paternal effort over mating effort.
As Strassmann notes, both the hypothesis developed by Alexander and Noonan
(1979) and her extension of that hypothesis have stood the test of time. There have
been alternative hypotheses presented, but Alexander himself was able to discredit
these hypotheses with a set of closely argued rebuttals in his own review of the
topic (Alexander 1990).
Strassmann devotes the rest of her introductory essay to examining the evi-
dence that ovulation is, in fact, concealed in humans. This claim has been the focus
of considerable attention in the literature, and a number of researchers have dis-
puted it. Strassmann provides an extensive and masterful overview of these stud-
ies, and shows that they do not provide convincing evidence against concealed
ovulation, when the phenomenon is properly understood. She brings to bear evi-
dence from the scientific literature, from her own ethnographic, behavioral and
physiological studies of the Dogon people of Mali, Africa (work of unparalleled
depth and detail), and from comparative studies across primates. This review sup-
ports the original claim of Alexander and Noonan (1979) that ovulation is indeed
concealed in humans, and that claims to the contrary are based on weak evidence.
She also critiques the assumption that any behavioral changes occurring over the
menstrual cycle are necessarily adaptive.

Eight

In chapter 8, Paul Turke introduces work by Alexander on a novel feature of human

primates—early-childhood physical altriciality coupled with psychological preco-
ciality— that has long withstood our understanding in terms of natural selection
 Introduction } 9

along the human lineage (Alexander 1990). This paper addresses the life-history
component of how modern humans have evolved, centering on how tradeoffs of
early survival with optimal trajectories of development to success as an adult have
been alleviated in humans by extensive parental care. Such shifts in life-history
selection (from just becoming a live adult, to becoming a better adult) thus freed
human infants to become physically helpless grubs that are neurologically highly
advanced over our ancestors. As for many other aspects of human evolution, a
complex Alexandrian mix of social cooperation with competition drives the life-
history transition to a long childhood, during which the social brain develops to
full, advanced maturity. Turke, an evolutionary anthropologist immersed in tra-
ditional cultures and their patterns of child-rearing, was a Postdoctoral Fellow at
Michigan with Alexander. He is now a (apparently, the world’s first) Darwinian
pediatrician, developing and applying evolutionary theory to help optimize child
development and health.

Nine

Chapter 9, introduced by Karl Sigmund, addresses a question that has puzzled

humans since the first written records of civilization: how and why humans
exhibit morality. Following in his mission to lay foundations for all characteris-
tics of humans, no matter how rarified or apparently problematic for evolution-
ary theory, Alexander (1987) expounds his concept of indirect reciprocity, which
extends from roots in nepotism and direct reciprocity to encompass interactions
between any and all pairs of humans, in any circumstance. As Sigmund, a leader
in the mathematical study of human social interaction, describes, this early work
by Alexander on the biological bases of indirect reciprocity, and its manifestations
as morality, has helped to inspire a now wide and deep field of game-theoretical
modeling that focuses on how humans cooperate and compete. This work, dove-
tailed with psychological and primatological studies, is uncovering the biologi-
cal underpinnings of human prosociality, and its dark sides of ingroup-outgroup
antipathy.

Ten

Robin Dunbar, one of the world’s leading thinkers on the biological and psycho-
logical bases for human sociality, introduces Alexander’s (1989) article on the evo-
lution of the human psyche. He sets this prescient paper into its theoretical and
historical context, as one of the first studies that comprehensively seeks to explain
the ”why” question of human consciousness and other core facets of the human
mind. As Dunbar describes, Alexander proposes the stunningly new hypothesis
that human mental capacities evolved in the context of selection for ability to
10 { Introduction

”play” in the mind—to build and permute, consciously and unconsciously, alter-
native social strategies and tactics in a world where evolutionary success is deeply
contingent on skills for social navigation. Language, brain size, the ”social” com-
ponents of the brain, complex cognition and affect, social-network structures,
the neurological ”default mode” system of functional brain activation—all follow
naturally from Alexander’s model for the evolution of the human psyche. Dunbar’s
work, like Alexander’s, is deeply rooted within primatological and anthropologi-
cal-archaeological contexts. This framework allows evaluation of how and why the
modern human lineage has so spectacularly diverged from all others, and what
this legacy may hold in store for, and suggest for improving, our runaway-tech-
nology future.

Eleven

Chapter 11 reprints a classic paper by Alexander (1982) on the evolution of moral-

ity. This subject represents the nexus of Alexander’s approach to human social
evolution, tying together a number of core themes that run through his work,
including family relationships, kinship networks, direct and indirect reciprocity,
ethics, law, justice, intergroup competition, warfare, and religious belief, with a
consistent focus on conflicts of interest. Alexander focuses on the conflict between
egoism and utilitarianism as a central paradox in moral philosophy, along with the
inherent duality of human nature.
David Lahti, a professor of biology at Queens College, City University of New
York, introduces the chapter. Lahti is eminently qualified to comment on the rela-
tionship between evolution and morality, as he holds doctorates in both evolution-
ary biology and philosophy and has published extensively on morality from an
evolutionary perspective (e.g., Lahti 2003). He begins his introduction by high-
lighting a long-standing conflict within the biology department at the University
of Michigan, in which Alexander and his students were seen as holding the view
that society is “built on lies.” This conflict traces to the extreme discomfort with
which many people (including many scientists) react to the concept of “human
interests” at the core of morality that Alexander’s evolutionary approach reveals.
Alexander begins the article by pointing out that previous attempts to analyze
morality have suffered from the lack of a proper understanding of human interests,
which ultimately center on efforts to promote the survival of the genes. Lahti notes
that this revelation comes as an unpleasant shock to many (himself included). He
then moves on to a brief but bracing review of the main objections of philosophers
to incorporating an evolutionary perspective into any analysis of morality. He
swiftly eviscerates some of the major objections to the evolutionary approach, and
yet makes a reasoned appeal for an important place for philosophy as we develop
an evolutionary approach to morality. Lahti then moves on to consider other
ways in which learning of Alexander’s detailed arguments relating evolution to
 Introduction } 11

morality might cause people to experience “nausea.” Alexander’s arguments imply

that moral behavior evolved in the context of egoism (actually inclusive fitness),
relative reproductive success, and intergroup competition (see ch. 6). Lahti points
out that each of these historical foundations shocks the typical moral philosopher.
But this is only the beginning of the discomfiture that Alexander’s world view can
engender. Alexander argues that an evolutionary view of morality explains why
justice is incomplete, why moral systems are not ideal, why happiness is elusive,
and why ethical dilemmas persist. Lahti notes that these views are anathema to
many; they find them depressing and nihilistic. From an evolutionary perspective,
every member of society has an interest in promoting moral codes that benefit
society as a whole (at an individual cost), even though they may not, in fact, follow
the code themselves. This kind of hypocrisy is (judging from virtually all sources
of news and gossip) extremely common, yet we continue to aspire to high moral
standards. Self-deception (in the service of deceiving others about our true inten-
tions) is rampant in this view, and may well be the norm rather than the excep-
tion. Hence, Lahti argues, it is not surprising that many, and probably most, have
responded to Alexander’s arguments with some mix of outrage, denial, accusa-
tions of bigotry (or worse), and general aversion. What then, are we to do, given
this window into our true natures (rather like the plastic windows inserted into the
sides of cows at the Cornell Veterinary School to reveal their intestinal workings)?
Alexander himself does not shy away from moral advice, even as he lays bare the
evolutionary roots of our moral codes in excruciating detail. Lahti argues that sev-
eral considerations may allow us to rescue morality from the primordial morass of
its evolutionary origins, although in every case there is no guarantee that our evo-
lutionary history will not, in fact, continue to influence our thinking and behavior.
Thinking about how to behave after coming to grips with Alexander’s evolutionary
understanding of morality is a bit like peering between two mirrors facing each
other. Nevertheless, Lahti elaborates three reasons that morality may well survive
the evolutionary onslaught on its perfection. He concludes by arguing in favor
of Alexander’s proposition that we are better off as a society and a species if we
understand the true evolutionary origins of our moralizing, rather than pretend-
ing that our moral codes are unsullied by the shadow of our evolutionary past.

Twelve

In chapter 12, Laura Betzig reviews the influence of the Alexander, Noonan, and
Crespi (1991) chapter on the evolution of eusociality (see also ch. 3), particularly
with regard to the importance of ecological constraints for human social evolu-
tion. Betzig, an evolutionary anthropologist, is particularly well qualified to com-
ment on this issue, as she has carried out extensive cross-cultural analyses of the
evolution of despotism and its relationship to differential reproduction in human
societies. She has written a book on the topic (Betzig 1986), has published many
12 { Introduction

more papers on the subject since, and is currently completing a book on the his-
tory of the West that also focuses on this issue. Betzig points out that the evolu-
tion of sterility that characterizes classical eusocial species such as ants and naked
mole-rats, has also applied to human societies (or to portions of them). Alexander
et al. (1991) emphasized the critical importance of ecological constraints in driving
the evolution of cooperative breeding, and ultimately (in the extreme) the sterile
castes of eusociality. This line of thinking can be traced to much-earlier papers by
Alexander, such as his classic 1974 paper on the evolution of social behavior (see
ch. 4). In turn, Alexander’s arguments in this vein led to the development of an
entire branch of theory within behavioral ecology (Reproductive Skew Theory; see
Vehrencamp 1983), as well as influencing the work of Betzig and others working
specifically on human behavioral ecology. As Betzig illustrates in her introductory
essay, the historical record strongly confirms the role of ecological constraints in
enabling despots to impose sterility on (some of) their subjects, across societies
and across the course of human history.

Thirteen

Stan Braude introduces chapter 13, an article by Alexander (1986) on the social-
evolutionary significance of one of the most curious facets of human social life and
language, humor. Braude, who was a doctoral student of Alexander’s studying naked
mole-rats, explains how Alexander’s attack on this topic epitomizes his belief that
evolutionary reasoning and analytic hypothesis-testing methods can and should be
applied to all human phenomena, even the most seemingly arbitrary and far-removed
from survival and reproductive functions. Alexander proposes and evaluates a suite
of ideas concerning the significance of humor in human social interactions—dis-
plays of social-linguistic prowess, ingroup-outgroup manipulations, tests of social-
intellectual skill, and strong links to mental scenario-building—all of which revolve
around his central thesis of shifting balances of social competition and coopera-
tion, at different levels, as prime movers of human evolution. Alexander’s analysis of
humor, unlike most of his other pioneering works, has yet to be built much upon by
others. Perhaps this is because he has reached so far in this case from biology into
everyday life, or perhaps it is because empirical tests of hypotheses for humor would
appear so challenging. We hope that the article will inspire such studies, to better
draw social biology, art, and language together, and understand a fundamental fea-
ture of what it means to laugh—and in doing so be human.

Fourteen

Chapter 14 presents an essay on the evolution of religion entitled “Religion,

Evolution and the Quest for Global Harmony,” which is published in this volume
 Introduction } 13

for the first time. This chapter is introduced by William Irons, a professor of
anthropology at Northwestern University, and a longtime friend and associate of
Dr. Alexander. His accomplishments in the field of evolutionary anthropology are
too numerous to recite here, but his contributions rank among the best in the field.
Irons has made substantive contributions to the study of religion from an evolu-
tionary perspective himself, having developed the hypothesis that deep religiosity
can serve as a signal of commitment to the group, one that is difficult or impossible
to counterfeit (Irons 2001). Irons points out that there have been two major themes
in the recent literature on the evolution of religion. A number of researchers have
focused on religion as a byproduct of psychological mechanisms that predispose
us to believe in unseen but imagined entities, such as gods. Research in this area
focuses on identifying aspects of our “environment of evolutionary adaptedness”
that might have selected for such tendencies, and on testing for specific psycho-
logical mechanisms in this context. Another group of related theories focus on
the idea that religious beliefs function to enhance cooperation among individuals
within groups. Irons places Alexander’s essay within the context of recent theory
in this area, and argues that his essay provides a novel approach that focuses on
the central values upon which religious belief and the ”concept of god” are based.
Alexander develops the idea that the concept of god serves as a metaphor for the
community at large, consisting of the “kindred” (an amorphous composite of all
an individual’s relatives, that shifts in composition based on individual perspec-
tive), and other individuals tied together through the bonds of reciprocity (direct
and indirect). In this sense, we have indeed evolved to “serve god,” as we serve our
circles of kin and friends, and this concept provides an evolutionary basis for the
origin and evolution of religious beliefs that is firmly based in inclusive fitness the-
ory, a foundation of evolutionary biology. Irons stresses a point also emphasized
by Alexander: It is not productive to denigrate other individuals for their religious
faith, and this conception of god and the meaning of religion may ultimately rec-
oncile scientific and religious views of the world.

Final

We introduce the final chapter, within which Alexander (2008) presents and evalu-
ates his hypotheses for how natural selection and human evolution have led to the
appearance, in modern humans, of art. Both of us received our doctoral degrees
at Michigan with Alexander as an adviser—and we both apparently imprinted
intellectually on him in following career paths that led from studies of behavior
and evolution of specific taxa (poison dart frogs and gall insects), to studies that
more or less directly address questions of human social evolution (e.g., despo-
tism, social-brain disorders, and others). We refer to the arts as the ”capstone”
of Alexander’s evolutionary edifice for explaining and analyzing human traits,
because in developing his theory for the arts he has, taken together with previous
14 { Introduction

work, conceptually unified virtually all human endeavors, including, arguably, the
most challenging and apparently far-removed from the machinations of natural
selection. Art is a reflection of culture. But, according to Alexander, it is also a
product of absorption and transmission of cultural entities by perceived inclusive-
fitness maximizing behavior, and a direct result of human scenario-building in
forged connections between minds. As such, art is beneficial, from an evolution-
ary perspective, to both artists and those who appreciate their creations. This bio-
logical basis for the arts should consummate the Darwinian syntheses of biology
with culture, science with the arts, and inclusive fitness theory with religion, com-
munity, and human well-being. Whether or not it truly does so will depend on
how Alexander’s ideas, here and in the previous chapters, are received and built
upon further. This will be up to you.
We conclude by arguing that many of the themes that Alexander championed
during his life’s work have become major subjects of interest and debate, and many
of his arguments have been amply supported by later work. For example, building
on Darwin’s (1871) argument that human cooperative tendencies developed in the
context of intergroup competition, Alexander developed the idea that intergroup
competition was a runaway process that ultimately led to the evolution of human
intellect and the primacy of social strategies in the evolution of intelligence (see
ch. 6 and its introduction by Low). The subject of intergroup competition and
warfare in relation to within-group cooperation in humans (and chimpanzees)
has recently become a hot topic, attracting both theoretical and empirical atten-
tion (e.g., Bowles, 2006, 2009; Puurtinen & Mappes 2009; Ginges & Atran 2011;
Matthew & Boyd 2011). Alexander’s focus on the importance of monogamy and
reproductive opportunity leveling in hominid evolution (see ch. 7 and its intro-
duction by Strassmann) is supported by recent results from the analysis of family
structure across hunter-gather societies (e.g., Hill et al. 2011).
It is now quite clear that, just as Alexander (1987) argued, reputation in the
context of indirect reciprocity has a profound effect on an individual’s treatment
by other individuals within their society (e.g., Milinski et al. 2002; Semmann et al.
2004; Nelissen 2008). Indirect reciprocity is a potent and viable mechanism for
maintaining cooperation, even in large societies (e.g., Nowak & Sigmund 1998;
Panchanathan & Boyd 2004; Rockenbach & Milinski 2006: see also ch. 9 and its
introduction by Sigmund). Key aspects of reputation building (or losing) such as
honor and heroism (and shame) have strong influences on human cooperative
behavior, just as Alexander predicted (e.g., Jaquet et al. 2011). Punishment, shun-
ning, and shaming are ubiquitous and potent components of human social inter-
action, providing powerful incentives to cooperate (e.g., Brandt et al. 2003; Price
2005; Barclay 2006; Rockenbach & Milinski 2006; dos Santos et al. 2011; Marlowe
et al. 2011). There is even evidence that individuals prefer to work in institutions
with substantial penalties for violating group norms, in the interest of ultimately
reaping higher rewards from participation (e.g., Gurek et al. 2006).
 Introduction } 15

Hence, it is quite likely that the fitness of individuals within social groups has
been closely linked to cooperativeness and willingness to contribute to group goals
over the long course of human history. This is not to say that intergroup competi-
tion has been unimportant in human evolution (quite the reverse), but there is
every indication that effective mechanisms of opportunity leveling (see ch. 2 and
Frank’s introduction thereto) including negative (shame, punishment, coercion)
and positive (reputation-based rewards, honors) mechanisms, have been highly
effective in aligning the interests of the individual with that of the group in human
societies.
In conclusion, there seems to be a consensus emerging that human cooperative
behaviors, and associated moral codes, have evolved through a delicate dance of
incentives (e.g., honor, recognition, and reward) and disincentives (e.g., punish-
ment, shaming, and shunning) among individuals who are balanced on a knife
edge of competition for hierarchy negotiation within groups and competition and
warfare between groups. This consensus is precisely what Alexander predicted in
his foundational body of work.

References
Alexander, R.D. 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5: 352–383.
Alexander, R.D. 1979. Darwinism and Human Affairs, Seattle: University of Washington
Press.
Alexander, R.D. 1982. Biology and the moral paradoxes. J. Social Biol. Struct. 5: 389–395.
Alexander, R.D. 1986. Ostracism and Indirect Reciprocity: The Reproductive Significance of
Humor. Ethol. Sociobiol. 7:253–270.
Alexander, R.D. 1987. The Biology of Moral Systems. Hawthorne, NY: Aldine de Gruyter.
Alexander, R.D. 1989. The evolution of the human psyche. Pp. 455–513 In C. Stringer and P.
Mellars (eds), The Human Revolution. Edinburgh, Univ. of Edinburgh Press.
Alexander, R.D. 1990. How Did Humans Evolve? Reflections on the Uniquely Unique
Species. Univ. Mich. Zool. Spec. Pub. 1: 1–38.
Alexander, R.D. 2008. Evolutionary Selection and the Nature of Humanity, Pp. 301–348 In
V. Hosle and C. Illies (eds), Darwinism & Philosophy. Notre Dame, IN: University of
Notre Dame Press.
Alexander, R.D. and Tinkle, D.W. 1968. A comparative review (of On Aggression and The
Territorial Imperative). BioScience 18:245–248.
Alexander, R.D. and Noonan, K. M. 1979. Concealment of ovulation, parental care
and human social evolution. Pp. 436–453 In: N. A. Chagnon and W. G. Irons (eds.)
Evolutionary Biology and Human Social Behavior: An Anthropological Perspective. North
Scituate, MA: Duxbury Press.
Alexander, R.D., Noonan, K.M., and Crespi, B. J. 1991. The evolution of eusociality. In:
Sherman, P., Jarvis, J.U.M, and Alexander, R.D. (eds.), The Biology of the Naked Mole-
Rat Princeton, NJ: Princeton University Press, pp. 3–44.
Barclay, P. 2006. Reputational benefits for altruistic punishment. Evol. Hum. Behav.
27:344–360.
16 { Introduction

Betzig, L.L. 1986. Despotism and Differential Reproduction: A Darwinian View of History.
New York, NY: Aldine-de Gruyter.
Bowles, S. 2006. Group competition, reproductive leveling, and the evolution of human
altruism. Science 314:1569–1572.
Bowles, S. 2009. Did warfare among ancestral hunter-gatherers affect the evolution of
human social behaviours? Science 324:1293–298.
Brandt, H., Hauert, C., and Sigmund, K. 2003. Punishment and reputation in spatial public
goods games. Proc. Roy. Soc. B 270:1099–1104.
Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: John
Murray.
dos Santos, M., Rankin, D.J. and Wedekind, K. 2011. The evolution of punishment through
reputation. Proc. R. Soc. B 278:371–377.
Flinn, M. and Alexander, R.D. 1982. Culture theory: the developing synthesis from biology.
Human Ecol. 10(3): 383–400.
Flinn, M. and Alexander, R.D. 2007. Runaway Social Selection in Humans. Pp. 249–255 In:
Gangestad, S. W. and Simpson, J.A. (eds). The Evolution of Mind. Fundamental Questions
and Controversies. New York: Guilford Press.
Ginges, J. and Atran, S. 2011. War as a moral imperative (not just practical politics by other
means). Proc. Roy. Soc. B 278:2930–2938.
Gürerk, Ö., Irlenbusch, B., & Rockenbach, B. 2006. The competitive advantage of sanction-
ing institutions. Science 312:108–111.
Hill, K.R., Walker, R., Bozicevic, M., Eder, J., Headland, T., Hewlett, B., Hurtado, A. M.,
Marlowe, F., Wiessner, P. & Wood, B. 2011. Coresidence patterns in hunter-gatherer soci-
eties show unique human social structure. Science 331:1286–89.
Irons, William. 2001. Religion as a Hard-to-Fake Sign of Commitment. Pp. 292–309 In:
R.M. Nesse (ed.), Evolution and the Capacity for Commitment. New York: Russell Sage
Foundation.
Jacquet, J., Hauert, C., Traulsen, A. and Milinski, M. 2011. Shame and honour drive coopera-
tion. Biol. Lett 7:899–901.
Lahti, D.C. 2003. Parting with illusions in evolutionary ethics. Biol. Phil. 18:639–651.
Marlowe, F.W., Bebesque, J.C., Barrett, C., Bolyanatz, A., Gurven, M. and Tracer, D. 2011.
The “spiteful” origins of human cooperation. Proc. Roy. Soc. B 278:2159–2164.
Matthew, S. and Boyd, R. 2011. Punishment sustains large-scale cooperation in pre-state
warfare. Proc. Natl. Acad. Sci. USA 108:11375–11380.
Milinski, M., Semmann, D. & Krambeck, H.-J. 2002. Donors to charity gain in both indirect
reciprocity and political reputation. Proc. R. Soc. B 269:881–883.
Nelissen, R.M.A. 2008. The price you pay: Cost-dependent reputation effects of altruistic
punishment. Evol. Human Behav. 29:242–48.
Nowak, M.A. and Sigmund, K. 2005. Evolution of indirect reciprocity. Nature 437:1291–98.
Panchanathan, K. and Boyd, R. 2004. Indirect reciprocity can stabilize cooperation without
the second-order free rider problem. Nature 432:499–502.
Price, M. 2005. Punitive sentiment among the Shuar and in industrialized societies: Cross-
cultural similarities. Evol. Hum. Behav. 26:279–287.
Puurtinen, M. and Mappes, T. 2009. Between-group competition and human cooperation.
Proc. Roy. Soc. B 276:355–360.
 Introduction } 17

Rockenbach, B. and Milinski, M. 2006. The efficient interaction of indirect reciprocity and
costly punishment. Nature 444:718–723
Semmann, D., Krambeck, H.-J. and Milinski, M. 2004. Strategic investment in reputation.
Behav. Ecol. Sociobiol. 56:248–52.
Strassmann, B.I. 1981. Sexual selection, paternal care, and concealed ovulation in humans.
Ethol. Sociobiol. 2:31–40.
Vehrencamp, S. 1983. A model for the evolution of despotic versus egalitarian societies.
Anim. Behav. 31:667–682.
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PART } I

General Foundations
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1}

Insect Behavior and Social Evolution

Phantasm
Soft staccato lisps of a bush katydid
Rising through cool mists of dusk
In a leftover lonely glacial spruce bog
High in the Appalachian Mountains
Quick insistent chirpings of brown field crickets
Across the moonlit landscape
Of a tiny hill prairie overlooking
Endless Mississippi River bottomlands
Eerily whining buzz of a great green
Grasshopper wafting on the wind
From far across the night-shrouded dunes
Alongside the lake named Michigan
Silvery tinkle of a miniature yellow cricket
Hidden in sun-speckled undergrowth
Of shadowy swamps across
The Everglades of Florida
Crashing synchrony of numberless cicadas
Chorusing deafeningly in the warm brightness
Of a June afternoon in open oak forests
Across the southeastern hills of Ohio
Lazy deep chir-ruping of a solitary beach cricket
Rising ghost-like in crashes of surf
Along a desolate rocky stretch
Of Atlantic coast at midnight
In such atmospheres I have imagined
I am the only human on earth, alone
A thousand centuries ago.
R. D. Alexander, 2011, p. 213
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 INTRODUCTION

From Cricket Taxonomy to a Darwinian Philosophy of Man

Mary Jane West-Eberhard

Figure 1.1 Singing male field cricket, courtesy of R. D. Alexander

Dick Alexander once recounted the story of a conversation with his mater-
nal grandfather, Noble Porter Heath II, an Illinois farmer, about his plan to go
to Australia to pursue taxonomic studies of the singing Orthoptera. “That’s a
long ways to travel on a cricket,” his grandfather quipped. This volume tells of
an intellectual voyage that went from a doctoral thesis on the taxonomy, sound
production, and classification of field crickets and cicadas, through studies of the
social behavior of insects and mole-rats, to seminal influential work on human
culture and morality—also a long ways to travel on a cricket.
Alexander’s path-breaking contributions to the study of human evolution did
not come out of the blue. They grew from an unusually acute understanding of
Darwinian evolution, that is, adaptive evolution by natural selection. He was
already a well respected evolutionary biologist—“distinguished” if we can judge by
several prominent awards—when he jumped wholeheartedly into the perpetual
fray of speculation about human evolution with a 1969 lecture on “The search
for an evolutionary philosophy of man” (Alexander 1971). His ability to see the
adaptive significance of major patterns in human behavior owes to his preparation
for this as a pioneer in Darwinian studies of nonhuman behavior. So looking at
his earlier work is important for understanding his innovative thinking about the
social behavior of humans and other animals.
The pioneer aspect of Alexander’s work, and the beginnings of a broad interest
in evolution, were evident in his graduate research in entomology at Ohio State
University. As a student of Donald Borror, Alexander was introduced to insect
24 { General Foundations

sounds as tools for the identification of species. But Borror used the characteris-
tics of insect songs as if they were morphological characters with no attention to
their functions or evolution, the aspects of most interest to Alexander even then:
“Function – behavior, and what it accomplished for the animal— was my first
interest” (RDA unpbl ms Autobiography IIIE, 2003).
Systematics has many virtues for understanding evolution. Among them is the
need for close attention to phenotypic variation and to the importance of genetics,
in particular reproductive (genetic) isolation, for producing the observed varia-
tion. Taxonomic research and fieldwork also promotes deep understanding of a
particular group of organisms, including its morphology, behavior, and natural his-
tory. Alexander’s earliest publications included articles on taxonomy that revealed
large numbers of cryptic species, and of previously unappreciated morphological
characters, based on studies of their acoustical communication (1957a), as well as
papers on sound production itself (1957b) and arthropod communication in gen-
eral (1960; 1964; 1967). The early publications grew increasingly broad in scope, as
they treated an expanding list of behavioral and life history phenomena as factors
in speciation (e.g., Alexander and Moore 1962; Alexander and Bigelow 1960) and
evolution (e.g., Alexander and Brown 1963).
Many of Alexander’s early papers appealed broadly to students of behavior and
evolution, including especially graduate students. My favorite is the now-classic
and still valuable monograph on cricket behavior, “Aggressiveness, territoriality,
and sexual behavior in field crickets (Orthoptera: Gryllidae)” (Alexander, 1961).
That paper documents the effects of male isolation, history of wins and losses, age,
size, and copulatory success on social rank, and it describes comparative studies of
mating behavior and sound communication, illustrating these phenomena with 63
figures, including photographs of behavior and audiospectographs of the calling,
fighting, and courting sounds of eight different species. The monograph ends with
a discussion of the evolution of social behavior in insects (see especially p. 212),
something that is surprising given the title of the paper, but not given the author.
It specifies how phenomena observed in crickets—evolutionary change in length
of adult life, and the transfer to females of communication morphology that origi-
nated in males—could affect the evolution of sociality in general: “Comparison
of the behavior of different species of field crickets and related Gryllinae suggests
some of the probable intermediate stages in the evolution of social behavior in
insects through an initial isolation of breeding pairs and their attachment to and
modification of particular localities” (p. 217).
Dick Alexander was a leader in promoting behavior as a taxonomic tool, but
went beyond that to emphasize the importance of behavior for understanding
adaptive evolution in general: “To paraphrase an old adage, it is not what one has
that counts in evolution, it is what one does with what one has—and what one does
is not always entirely clear from what one apparently has,” meaning morphology
alone (Alexander 1962a). He once brought an antique apple peeler to class and
asked what we guessed its function might be. The gadget had a number of puzzling
 Insect Behavior and Social Evolution } 25

complicated parts, but their functions were clear once an apple was attached and
the handle turned.
A 1962 article in Evolution on “Evolutionary change in cricket acoustical
communication” (Alexander 1962b) could serve as a model of how insightful,
detailed comparative study of phenotypes—behavior, ontogeny, sex differences
and ecology—can be used to make deductions regarding evolution without fos-
sils and without explicit genetic data, using indirect evidence of genetic diver-
gence. These early publications emphasized the use of behavior as the secret to
understanding adaptive significance, and the search for adaptive significance as
the secret to understanding behavior. It is obvious that such lines of thinking
were important for developing ideas about human evolution. They show how
Alexander’s bold breach of the boundary between biology and the social sci-
ences grew from a background in taxonomy, a field where orderly and essen-
tially conservative practices prevail and expertise is often deep but circumscribed
within what has been called the “comfortable separateness” of a specialized field
(Anonymous, 2011). Notable for reaching beyond such boundaries, the 1962 paper
on “The Role of Behavioral Study in Cricket Classification” (Alexander 1962a),
presented at a 1961 meeting of the American Association for the Advancement of
Science, won the AAAS Newcomb Cleveland Prize for an “outstanding contribu-
tion to science.”
The scientific values that grew out of Dick Alexander’s early work deeply influ-
enced his later research and that of his students, who, like me, took those values
as their own. One of them is a consuming passion for work on a particular group
of organisms, with a determination to learn all that is known about it—a commit-
ment to taxon-centered research whose merits I have discussed elsewhere (West-
Eberhard 2001). Concentrating initially on evolutionary questions in a particular
group of organisms always reveals something of general interest. And it quickly
makes a beginner into an expert ready to tackle larger questions, with a concrete
basis for critical thinking on almost any major topic in evolutionary biology. It
also fosters confidence in one’s ability to make an original contribution of some
importance. In Dick’s case the originality and breadth of his comparative studies
of the singing insects made him quickly recognized as an expert on the evolution
of animal communication and its role in systematics and speciation. From there
it is not so difficult to embark on comparably original work on the evolution of
humans.
Still, one might wonder: What would motivate a scientists trained as an ento-
mologist to turn from successful work on six-legged creatures to confront the
complex and controversial world of research on human evolution? This question
has been answered by Alexander himself, in a biographical essay (Alexander 2009,
p. 23):

How and why did I make the transition, initiated around 1967, from study-
ing the singing insects as a systematist and behaviorist to eventually writing
26 { General Foundations

some 50 articles and two books about how evolution applies to humans and,
in particular, human behavior? I decided in 1954, the day after I passed the
written and oral preliminary examinations for the doctorate, that I wanted
to be an evolutionary biologist. A few years later I realized I would like to
think of myself (grandly!) as trying to falsify the hypothesis that everything
about life is a result of evolution, . . . The approach I set for myself would
require that I proceed eventually to the most difficult of all traits (behavior)
and the most difficult of all species (humans).

The excerpts reprinted here are from “Comparative animal behavior and sys-
tematics,” (1969), the published version of a 1967 lecture given at an international
conference on systematic biology convened by the National Academy of Sciences
in Ann Arbor. It represents a clear bridge between the early papers on behavior
and systematics and the later ones on humans. This is the paper that Alexander
himself recognizes as the turning point in his commitment to put human evolu-
tion at the center of his research (Alexander 2009). Even though the lecture was
presented at a symposium on the classification of organisms, it is really an essay on
adaptive evolution and the urgency of extending modern Darwinian thought to
studies of human behavior. Following some brief introductory remarks on behav-
ior and systematics, the paper moves abruptly to a section headed “Behavior and
Man’s Evolution,” with a single transitional sentence: “The facts I have outlined
above suggest some of the problems and possibilities in using behavior to under-
stand the history of life. I think one of the best illustrations of these problems and
possibilities comes from the evolution of man himself ” (p. 495).
With that sentence Alexander began more than four decades of research
devoted to understanding human behavior and the evolution of sociality. The
excerpts reprinted here emphasize the general principles of adaptive evolution that
inspired Dick Alexander, and through him others, to give studies of human evolu-
tion a solid Darwinian base.

References
Alexander, R.D. 1957a. The taxonomy of the field crickets of the eastern United States
(Orthoptera: Gryllidae: Acheta). Ann. Entomol. Soc. Amer. 50(6):584–602.
Alexander, R.D. 1957b. Sound production and associated behavior in insects. Ohio J. Sci.
57(2):101–113.
Alexander, R.D. 1960. Sound communication in Orthoptera and Cicadidae. In: W. E.
Lanyon and W.H. Tavolga (eds.), Animal Sounds and Communication, AIBS Publications
7:38–92.
Alexander, R.D. 1961. Aggressiveness, territoriality, and sexual behavior in field crickets
(Orthoptera: Gryllidae). Behaviour 17:130–223.
Alexander, R.D. 1962a. The role of behavioral study in cricket classification. System. Zool.
11(2):53–72.
 Insect Behavior and Social Evolution } 27

Alexander, R.D. 1962b. Evolutionary change in cricket acoustical communication. Evolution

16(4):443–467.
Alexander, R.D. 1964. The evolution of mating behavior in arthropods. Symp. R. Entomol.
Soc. Lond. 2:78–94.
Alexander, R.D. 1967. Acoustical communication in arthropods. Annu. Rev. Entomol.
12:495–526.
Alexander, R.D. 1969. Comparative animal behavior and systematics. In: Systematic Biology.
Proceedings International Conference on Systematics (Ann Arbor, Michigan, July 1967).
National Academy of Sciences Publication 1962: 494–517.
Alexander, R.D. 1971. The search for an evolutionary philosophy of man. Proc. R. Soc.
Victoria 84:99–120.
Alexander, R.D. 2009. Understanding ourselves. In L.C. Drickamer and D.A. Dewsbury
(eds.), Leaders in Animal Behaviour: The Second Generation. Cambridge: Cambridge
University Press, pp. 1–37.
Alexander, R.D. 2011. The Mockingbird’s River Song: Poems, Essays, Songs and Stories, 1946-
2011. Manchester, MI: Woodlane Farm Books.
Alexander, R.D. and Bigelow, R.S. 1960. Allochronic speciation in field crickets, and a new
species Acheta veletis. Evolution 14(3):334–346.
Alexander, R.D. and Brown,W.L. 1963. Mating behavior and the origin of insect wings. Univ.
Mich. Occas. Pap. 628:1–19.
Alexander, R.D. and Moore, T.E. 1962. The evolutionary relationships of 17-year and 13-year
cicadas with three new species (Homoptera: Cicadidae: Magicicada). Univ. Mich. Mus.
Zool. Misc. Pub. 121:1–59.
Anonymous, 2011. Editorial statement. Daedalus 140(1):1.
West-Eberhard, M.J. 2001. The importance of taxon-centered research in biology. In M. J.
Ryan (ed.), Anuran Communication. Washington, DC: Smithsonian Institution Press,
pp. 3–7.
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 COMPARATIVE ANIMAL BEHAVIOR AND SYSTEMATICS

Excerpt from Alexander, R. D. 1969. Comparative animal behavior and sys-

tematics. In: Systematic Biology. Proceedings of the International Conference on
Systematics (Ann Arbor, Michigan, July 1967). National Academy of Sciences
Publication 1962: 494–517.
Behavior is probably the most diverse aspect of the animal phenotype—at least,
as William Morton Wheeler (1905) put it, “in the field of possible observation.” On
this basis alone, behavior should be fascinating to the systematists because they
are always looking for characters. Furthermore, among biologists, systematists are,
more than any other group, the real students of diversity. Comparison is their chief
method of exploration, and the comparative method, of course, depends upon and
thrives upon diversity.
On the other hand, to some extent the diversity of behavior results from its
being, in general, more directly and probably more complexly related to the geno-
type than to any other aspect of the phenotype. This particular feature discourages
the systematists. They are not interested in getting involved with phenotypic varia-
tions that might be due solely to variations in the developmental environment.
After all, morphology is troublesome enough in that regard.
Behavior has some other special features. In general, it is more strongly
selected—or perhaps I should say more directly selected—than morphology
or physiology. By this I mean that in any representation of the chains of cause-
effect relationships between gene action and selective action in animals, behav-
ioral characteristics nearly always would be placed directly next to selective
action.1
The systematist’s concern with adaptation should prevent him from passing
this off too lightly. On the other hand, behavior is often difficult to document or
to communicate to others. As Dr. Wagner stressed in his paper, repeatability is
the essence of science, and to many taxonomists this traditionally has meant that
morphology alone is sacred. Very little behavior is evidenced by preserved speci-
mens or fossils.

1
A botanist asked me abruptly in a phone conversation recently, “What is animal behavior, any-
how?” I tried to answer him unhesitatingly, and my reply came out: “Behavior is what animals have
interposed between natural selection and the other (morphological and physiological) aspects of their
phenotypes.” Even with an indefinite amount of reflection, I think it might be difficult to improve on
the emphasis in that definition.)
30 { General Foundations

Behavior and Man’s Evolution

The facts I have outlined above suggest some of the problems and possibilities in
using behavior to understand the history of life. I think one of the best illustrations
of these problems and possibilities comes from the evolution of man himself. We
surely would all agree that the most important thing we could possibly discover
about man’s transition from the nonhuman state to the human state would be how
he behaved during that period—the details of what he did and how he lived while
he was evolving into a man. We know positively that he did make the transition
from ape to man. What we do not know is precisely how he did it. By that I mean
we do not know what the selective forces were, and, for example, why such forces
seem to have been relatively strong and unidirectional for a while—at least in
regard to changes in size of the brain case—and then to have slacked off, perhaps
rather abruptly, some tens of thousands of years ago. We speak (vaguely, I think) of
tools and communication, and of growing food and fighting off predators, but the
truth is we still have no really good notion how and why men with bigger brains
once outreproduced those with smaller brains and then stopped doing so.
A wide range of possibilities still exists, and the answers could very well turn
out to be more startling than most of us might suppose. As one example, we
do not really know what kinds of predators, if any, might have been involved in
the steady increase in man’s brain size, and, as much as we may dislike the idea,
I believe the possibility still exists that man himself is the only one that could have
done the job.
Perhaps I can explain what I mean, and demonstrate some of our ignorance
about man’s evolution, by posing a question. Intraspecific competition, in con-
nection with natural selection, may be said to occur in three possible forms.
Sometimes different individuals simply compete indirectly, without direct interac-
tions, for whatever food, mates, shelter, or other commodities may be in short sup-
ply. In other cases, some kinds of individuals may partially or completely exclude
others from the best sources of food, mates, and shelter through territoriality of
one sort or another. There is another possibility, less often recognized. Superior
individuals might sometimes actually pursue and destroy competitors, or poten-
tial competitors, thus removing them and their descendants from the possibility
of competing. Such a superior individual might, in addition to removing com-
petition, actually derive direct benefit from the slaughter, through cannibalism.
Which of these three kinds of intraspecific competition operated during the evo-
lution of humans from nonhuman primates, and how significant was each? The
question has certainly not been answered; I do not think it has even been clearly
posed before. Yet the different possibilities could scarcely fail to produce widely
different attitudes among men trying to understand themselves and their behav-
ior through knowledge of history. [Since submission of this manuscript the ideas
involved here have been discussed and extended in a book review coauthored by
D. W. Tinkle (Bioscience 18:245–248).]
 Insect Behavior and Social Evolution } 31

Sometimes I have thought that to understand the selective action that made
a nonhuman primate into a man could be the most important question in all of
biology. It could change man’s attitude toward nearly everything he does or tries
to do—in education, politics, religion, and all the rest—for it could tell him more
precisely what he is, and therefore why, in one sense, he persists in doing some
of the things he does, and why he still fails to accomplish some of the things he
seems to want to do. Any adult who has tried to explain to a child the pre-emi-
nence of things sexual in so much of human affairs (as well as in the lives of other
organisms) without using natural selection in his explanation surely will under-
stand what I mean. To use another example, it is possible that we should be taking
the history of selective action upon man much more directly into account in our
attempts to deal with overpopulation and its consequences.
In other words, we cannot learn how man became a man, and therefore, in a
sense, what a man really is, without knowing some things about the history of his
behavior. Yet, it seems that the only thing we can do about this problem is to dig
and scrape around at a few fossils that reflect his morphology and represent a few
indirect traces of his behavior.

The Comparative Method In Behavior

It seems as though this is all we can do; but my theme here is that such an idea
about evolution is false. I suggest that we can find out how man’s behavior evolved
and the kinds of selective action that were involved. More fossils will help, of
course, but we can do it without fossils if we have to; in any case, the most impor-
tant advances in understanding man’s history may not come from fossil evidence,
and I consider it unlikely that satisfactory progress will come from the efforts of
humanists who are not simultaneously first-rate evolutionary biologists. I believe
that we will make the significant advances in this area in the same way that we
eventually would have arrived confidently at the conclusion—even without the
help of a single fossil—that man and the other living primates have diverged from
common ancestors. We would have done this, of course, through extensive, inten-
sive, and perceptive comparative study over a period of time long enough for us to
have developed—on the side, from direct observation and experimentation—an
understanding of the steps and the mechanics of the process of evolution.
It should be clear by now that I am not arguing simply about the role of behav-
ior as a tool for taxonomists. I want to argue instead for the establishment of a
reasonable relationship between those biologists interested primarily in behavior
and those interested primarily in systematics in the broadest sense—a relation-
ship that will result in the kind of reverberating feedback between these fields
that both need, and have needed, for a long time. I think the key to this relation-
ship—perhaps the only key—lies in applying the comparative method to behavior
on a much wider scale than has been the case. I realize that I am one small voice in
32 { General Foundations

a long line of people carrying this particular argument to the zoologists. But I do
think the point has not yet been properly made.
To some zoologists—though perhaps not to those here—to argue for a rejuvena-
tion of comparative study must sound a little old-fashioned. Nowadays biologists
are calling for precise, quantitative results and for more and more experimenta-
tion. Comparative study and the broad-scale, observational-descriptive work that
undergirds it are often viewed as outdated, trivial pursuits. The need for more
experimental work, however, and the possibility of more precise experimentation
do not reduce the need for good, evolutionarily oriented, comparative investiga-
tions. Rather, though it may surprise some biologists, the need for comparative
study is thereby increased, for it is a central role of comparison to tell us which
experiments to do, and which ones to do first.
In his recent book on adaptation and natural selection, Williams (1966a) argued
that systematists never will prosecute the study of adaptation the way it ought to be
prosecuted. All of us will agree that there is a lot of shortsighted, narrow-minded
systematic work going on but, contrary to Williams’ argument, I believe that the
methods of systematists represent a great potential contribution to the study of
adaptation, beginning at the point where we find ourselves today. And I refer spe-
cifically to the comparative study of behavior, which Williams himself employed
effectively in his book. Comparative study is the stock-in-trade of the systematist.
It has never been the stock-in-trade of any other group of biologists in a very
extensive, persistent, or pertinent fashion—least of all, perhaps, the behaviorists.
One of my favorite psychologists argued recently that molecularly oriented
biologists are on the wrong track when they believe they can predict everything
of significance about the biological world through a knowledge of structure and
function at molecular and submolecular levels. He noted that, while theoretically
this may be possible, it is unreasonable or impractical unless one knows before-
hand what it is that he must be able to predict. I suggest that the same criticism
can be leveled at many people studying behavior. They expect to be able to predict
from precise, quantitative, laboratory experimentation without having any idea
of the complexity, the variety, or even the nature of the things they will have to
predict.
Zoologists left behavior largely to the psychologists, long past the time of know-
ing that psychologists in general do not answer the kinds of questions that zoolo-
gists must have answered. And systematists, in turn, have left zoological studies
of behavior to the experimental zoologists, despite the fact that certain questions
about behavior that are of importance to everyone are not going to be answered for
a very long time using the methods generally conceded to experimental biology.
There is nothing mysterious about the comparative method. Yet I am convinced
that many systematists and other biologists who use it all the time scarcely know
what they are accomplishing with it, are not sufficiently prepared to explain and
defend its problem-solving value, and, in any case, could not give a clear exposi-
tion of its usefulness to systematics or to biology in general.
 Insect Behavior and Social Evolution } 33

The Problem of Instinct

So far, I have said nothing about what undoubtedly has been the knottiest prob-
lem in the study of animal behavior, and the one responsible more than any other,
I suppose, for slowing the advance of comparative study of behavior. If we call this
the “problem of instinct,” most people have a good idea what is meant. It would
be more descriptive, however, to term it the problem of the extent and nature of
hereditary influences in behavioral variations, both between species and among
the individuals of each species.
Adaptation is a result of selective action on alternative genetic phenomena.
Therefore, it is critical for my topic to determine which behavioral variations cor-
relate with genetic variations. Few people challenge the idea that certain species
differences, such as frog and insect calls, firefly flashes, or other behavioral charac-
teristics identified as reproductive isolating mechanisms in any kinds of animals,
have genetic bases. And, we know from hybridization experiments that insect and
anuran call differences do indeed have genetic bases. In fact, results from crossing
experiments on crickets and frogs probably are cited more frequently in reviews
concerning transmissibility of behavioral variations than are any experiments with
other kinds of animals.
The systematist wants to know more about this. He wants to know whether he
can be sure that he is not examining some behavioral difference that has noth-
ing to do with hereditary differences. Some systematists and other biologists have
gotten involved in long, bitter, and futile arguments about whether heredity or
environment has greater influence in determining the characteristics of particular
behavior patterns.
Concerning this topic, we are pursued now by a whole string of admonish-
ments: “To ask how much a given aspect of behavior depends upon genetic fac-
tors and how much upon environmental factors is like asking how much of the
area of a field depends upon its length and how much upon its width”; “Nothing
is inherited but the genotype and a little cytoplasm”; “Heredity is particulate; but
development is unitary”; “Instead of speaking of this or that trait as genetic or
environmental, the correct way is to ask yourself which, and the extent to which,
differences in characters are due to environment on the one hand and to heredity
on the other.”
Konishi (1966) has recently written a paper that, I think, clarifies some issues
Involved in this problem. He points out that, as one of our shortcomings, we have
acted as though it is always true that, in behavior, stereotypy = species specificity =
inheritance = central coordination = spontaneity = self-differentiation. These fac-
tors are not strictly correlated and, as with learning, what has been called “instinc-
tive” behavior really is not a single phenomenon, and it should not be treated as
if it were.
But not all these issues are of great or immediate concern to the systematist or
evolutionary biologist interested in behavior. What is of concern is predictability.
34 { General Foundations

And it is very likely that significant increases in predictability, in many cases, can
be attained sooner by insightful, properly directed, broad-scale (even superficial)
comparisons than by detailed studies of development of specific patterns of behav-
ior in individual animals or species. The comparative anatomists, as many etholo-
gists have emphasized, have already shown this to be true. We systematists seem to
have allowed ourselves to be overly concerned about precisely how individual pat-
terns of behavior develop. We do not know a great deal about the development of
morphology in a wide variety of animals; but we do know a very great deal about
speciation, adaptation, and phylogenetic history—all of which knowledge was
gained directly, almost solely, from comparisons of those very features of anatomy
whose development we still do not understand.
When we will have carried out broad-scale comparative studies of behavior
similar to those available in anatomy, and when we begin to acquire the glim-
mers of understanding that will come from predictiveness based on such studies,
then those investigators concerned chiefly with the developmental bases of phe-
notypic differences will, indeed, have something to think about and work with.
Because the question then would concern how much genetic variation is involved,
a considerably sharper focus should be provided for the investigations of many
biologists now skeptical that broad-scale comparisons can be made in the absence
of extensive information on developmental pathways and stimuli for particular
behavioral units.
This remark may raise some eyebrows, but I suggest that behavioral variations
that at first glance appear useful to systematists—particularly to those working
at and above the species level—rarely lack correlation with specific genetic varia-
tions. For example, is anyone here in a position to describe a species difference in
behavior—any species difference in behavior—that he has cause to suspect does
not have a genetic basis? 2
Further, and of great importance, the extent and nature of correlations between
behavioral variations and genetic variations—or their absence—is predictable to
a large extent.
One aspect of such predictability can be exemplified by cricket calls. Examination
of cricket biology soon reveals that in most temperate species only the eggs pass
the winter, and that the auditory organs are not functional until maturation or
near-maturation. With this information alone we can predict confidently that (at
least usually) selection favors insulation from influences by environmental sounds
in the establishment of the pattern of the call (R. D. Alexander, “Arthropods” in
T. Sebeok, Animal Communication, to be published by Indiana University Press),
for there can be no appropriate sounds available to copy.

2
Alexander and Bigelow (1960) have given a possible example. Males of Gryllus veletis generally
are much more aggressive than those of G. pennsylvanicus. They also occur more sparsely, and the dif-
ference can be erased, or even reversed, if males of G. veletis are crowded in the laboratory and males
of G. pennsylvanicus are isolated.
 Insect Behavior and Social Evolution } 35

On the other hand, even a limited knowledge of passerine-bird biology allows

the reverse prediction: that most young birds probably have evolved specific ways
of being influenced by their parents’ song patterns. There are at least two reasons:
the overlap of young and adults in each generation, and an apparent premium on
individuality in song pattern; the latter is associated with the presence of special-
ized parental behavior and tendencies toward monogamy and is promoted by hav-
ing part of the pattern learned.
In precocious birds both the critical periods of song learning and the imprint-
ing of following behavior are predictable on the same general basis. Even the
indiscriminateness of suitable stimuli for imprinting of following behavior is pre-
dictable, for the situation is such that unsuitable stimuli are not likely to be avail-
able, and selection, therefore, will have no chance to focus on a restricted group
of stimuli. Likewise, we would predict that different populations of birds within a
given species should sometimes have song differences that lack genetic bases, as is
the case with human languages.
The psychologists who chastised ethologists for erecting dichotomies with
regard to learned and unlearned behavior were right, for many ethologists had
their dichotomies out of focus. But this argument became a source of confu-
sion rather than clarification when it took the form of rejecting all implications
of important dichotomies in the way behavior patterns develop. An important
dichotomy can be identified in the examples I have just given: Does the selection
favor the use of a given stimulus (sound, for example) in the establishment of a
pattern in the same modality as the stimulus or does it specifically favor insulation
from all stimuli in that particular modality? This is a dichotomy as to direction
of selection, and it leads to extreme differences in certain relationships between
genetic phenomena and behavioral characteristics. We identify it and discover its
significance by studying adaptation and natural selection in relation to behavioral
development.
I suggest that selection acting consistently on any kind of behavioral varia-
tion, regardless of its original basis, will usually result in the presence, ultimately,
of genetic variation that relates directly to the behavioral variation. This would
mean that the more ancient a behavioral difference, the more likely it is to have
some genetic basis. By this I do not mean to imply any special kind of selection,
I simply mean that selection will work on both genetic and non-genetic varia-
tions, but evolution will occur only when genetically based variations become
available.
No broad-scale attempt has been made to study adaptation in behavioral terms
by the kind of comparison and prediction that I have just described. Yet, if what
I have argued is true, such attempts would be fruitful, even those dealing with
the behavior of man, of all organisms the most “labile” in the functioning of his
phenotype.
I will use a simple example cited by Williams (1966a), who notes that the
females of many kinds of animals usually are described as being more “coy” or/
36 { General Foundations

discriminating or reluctant in copulation than the males (or one could turn it
around and say that the males are more “aggressive” in courtship), and he notes
that this is predictable because in each copulation or fertilization the female invests
a greater proportion of her total reproductive potential than the male invests of
his. If this argument is correct, then, as Williams points out, the situation should
be reversed in parental animals in which the male is solely responsible for the
zygotes, or more involved in parental behavior. Such reversals have been reported
in pipefishes in the genus Syngnathus, in which the males carry the fertilized eggs
(Fiedler, 1954), though not in all such fish (Breder and Rosen, 1966; Straughan,
1960), and also in such birds, as some tinamous and phalaropes, in which the males
incubate the eggs and protect the young (Bent, 1927; Tinbergen, 1935; Höhn, 1967).
Similar reversals as to which sex behaves territorially, fights off intruding indi-
viduals, and courts more aggressively have been reported in the ornate tinamou
(Pearson and Pearson, 1955), red phalarope, northern phalarope, and Wilson’s
phalarope (Tinbergen, 1935; Höhn, 1967; Bent, 1927). Polyandry is more likely to
be prominent in such animals, and strict polygyny ought to be rare, although both
polygamy (or promiscuity on the part of both sexes) and monogamy have been
reported (Lancaster, 1964; Höhn, 1967). Polygyny, on the other hand, is prominent
among species in which the females carry most or all of the parental responsibility,
and polyandry is almost nonexistent. Some of the disagreements in the literature
(e.g., see Höhn, 1967) may result from differences in sex ratios among demes stud-
ied by different investigators. In some cases, what happens when sex ratios are
locally or temporarily uneven may be important in understanding how selection
has operated.
The relationship between reproductive effort and proportion of reproductive
potential involved in any circumstance or event can be extended to include not
only the proportion of eggs or sperm used per copulation but also the proportion
of the breeding season used per clutch or pregnancy and the proportion of the
total probable reproductive life involved in each season, as Dr. Tinkle demon-
strated on this program. Such considerations of proportions must include also the
likelihood of changes in reproductive possibility—such as improvements through
learning about one’s mate or about the food and predators in one’s territory—and
the likelihood of improvement in weather conditions. Williams (1966b) and Lack
(1966) have pointed out that this means that longer juvenile lives will correlate
roughly with longer reproductive lives, and that clutch sizes will increase with age.
We should expect, especially in long-lived, monogamous animals with special-
ized parental behavior, that selection continually will maximize the slope of a line
depicting the increasing reproductive ability of individuals and pairs.
Since man’s plasticity in behavior seems for a long time to have been a major
reason for our reluctance to discuss the general problem of behavior in relation
to heredity and, therefore, a major reason for the reluctance of systematists and
other biologists to use behavior in comparative work, it is appropriate that I con-
clude by referring to the possibility of heredity in an example of variation in man’s
 Insect Behavior and Social Evolution } 37

behavior. I will use the previously mentioned theory of female “coyness,”; or dif-
ference between male and female, and suggest that what we frequently and some-
times jokingly refer to as the “double standard” in man’s sexual behavior is, in part,
a reflection of differences in selective action on male and female behavior during
man’s evolutionary history.
In general, in both polygynous and monogamous animals with specialized
parental behavior, selection should favor females that promote monogamy and
should favor males that promote polygyny. Even in evolutionary lines in which
monogamy is never actually realized, tendencies toward it in females would be
favored consistently if the male’s cooperation in any way promoted the female’s
reproductive success. Likewise, even in a monogamous line polygynous tenden-
cies in males often would be favored because in a species in which the female is
responsible for the fertilized eggs a male is much more likely to benefit from, shall
we say, “stealing” copulations with his neighbors’ females than is the female who
indulges in the same kind of behavior. Tendencies toward polyandry in man are
evidently rare, but tendencies toward polygyny are not nearly so rare.
Is it reasonable to argue that there likely are no genetic correlates underlying
even subtle intraspecific differences of this sort in an organism as plastic as man,
when selection on man’s breeding system has probably been consistent in the ways
I have described all through man’s evolutionary history? I think not.

Concluding Remarks

I have dealt in this paper with a few points that I believe will be useful in making
the analysis of behavior more important in systematic work than it has been in
the past, in searching for both similarities and differences among organisms. To
bring these two fields into closer cooperation, I believe we need, chiefly, to be (1)
more aware of the role of the comparative method in biology and in behavioral
analysis, (2) more thoughtful in our searches for behavioral variations likely to be
correlated with genetic differences, and (3) as systematists, more cognizant than
we have been of the significance of studying adaptation directly, both by experi-
mentation and by comparison.

Acknowledgments

I wish to thank Daniel Otte, Ann Pace, and Mary Jane West, graduate students at
the University of Michigan, for assistance in developing the ideas presented here
and for critical examination of the manuscript at various stages.
38 { General Foundations

References
Alexander, R.D. and Bigelow, R. 1960. Allochronic speciation in field crickets, and a new
species Acheta veletis. Evolution 14:334–336.
Bent, A.C. 1927. Life Histories of North American Shore Birds. Part 1. Washington, DC:
US National Museum Bulletin 142.
Breder, C.M. and D.E. Rosen, 1966. Modes of reproduction in fishes. Neptune City, NJ:
T.F.H. Publications.
Fiedler, K. 1954. Vergleichende verhaltenstudien an seenadeln, schlangennadeln und
seepferdchen(Syngnathidae). Z. Tierpsychol. 11:358–416.
Höhn, E.O. 1967. Observations on breeding biology of wilson’s phalarope (Steganopus
tricolor) in central Alberta. Auk. 84:220.
Konishi, M. 1966. The attributes of instinct. Behaviour 27:316–327.
Lack, D. 1966. Population Studies of Birds. Oxford: Clarendon Press.
Lancaster, D.A. 1964. Life history of the Boucard Tinamou in British Honduras. Part II:
Breeding Biology. Condor 66:253–276.
Pearson, A.K., and Pearson, O.P. 1955. Natural history and breeding behavior of the
tinamou, Nothoprocta ornata. Auk 72:113–127.
Straughan, R. P. L. 1960. 100 seahorses spawn. Aquarium J. 31:302–308;325–326.
Tinbergen, N. 1935. Field Observations of East Greenland Birds. I. The Behaviour of the
Red-Necked Phalarope (Phalaropus lobatus L.)in Spring. Ardea 24:1–42.
Wheeler, W. M. 1905. An interpretation of the slave-making instincts in ants. Bull. Am. Mus.
Nat. Hist. 21:1–16.
Williams, G.C. 1966a. Adaptation and Natural Selection. Princeton, NJ: Princeton University
Press.
Williams, G.C. 1966b. Natural selection, the costs of reproduction, and a refinement of
Lack’s principle. Am. Natur. 100:687–690.
2}

Cooperation

About the Social Contract

Am I an outlaw, you ask? Am I?
Tell me which rules of this desperately
social beast whose genes I share must be
forgotten, ignored, or despised for me to qualify.
Tell me the shape of the particular horrors I
personally must plunge into a man’s eye,
how I must shave my ideas or my
hair to stay out of that No-Baboon’s Land,
and why.
Explain to me the times when my
personal conscience cannot fly
in the face of the social ones of this time
or that, concerning who must die,
and in what order.
Tell me whom I may or may not love, and why.
Say how much of me will be permitted to identify
with the unusual dreams of one whose eye
may seem to see it all differently. Apply
your (or is it “our”?) laws, and I
will give you my reply.
And why.
Or have I?
Alexander 2011, p. 20
 INTRODUCTION

A New Theory of Cooperation

Steven A. Frank

The function of laws is to regulate . . . the reproductive strivings of individuals

and subgroups within societies, in the interest of preserving unity in the larger
group. . . . Presumably, unity in the larger group feeds back beneficial effects to
those . . . that propose, maintain, adjust, and enforce the laws.

alexander 1979, p. 240

A corollary to reproductive opportunity leveling in humans may occur through

mitosis and meiosis in sexual organisms. . . . The leveling of reproductive
opportunity for intragenomic components . . . is a prerequisite for the remarkable
unity of genomes.

alexander 1987, p. 69
When I first read Alexander’s (1987) The Biology of Moral Systems, I was stunned to
find a truly new theory of biological cooperation. I had thought of the theory of social
evolution as an already mature subject, fully developed with regard to fundamental
concepts. Yet, in Alexander’s book, I could see a completely new way to think about
social evolution. In this essay, I explain that new theory and where it came from.
Dick Alexander, Bill Hamilton, and Bob Axelrod taught me the classical theory
of social evolution at the University of Michigan in the late 1970s and early 1980s.
That classical theory provided two explanations for cooperation: kin selection and
reciprocity. At that time, the theory seemed mature and complete with regard to
setting the foundation for the field. I hardly expected to come across a totally new
way of thinking about the evolution of cooperation.
Yet the main weakness of the theory was also apparent. Extensive cooperation
occurs between nonrelatives. Different genes in genomes are functionally inte-
grated but not related. Larger human societies often have many highly cooperative
but distantly related individuals. Some of this cooperation between nonkin can
be explained by extensions of reciprocity to a general notion of mutual benefit for
interacting partners (West-Eberhard 1975). In the early 1980s, kin selection plus
these extended notions of reciprocity were the main conceptual tools.
Those limited conceptual tools led to blind spots about unsolved problems.
Only rather forced theories of mutualism could work for the nearly complete
 Cooperation } 41

integration of genes into cooperative genomes. Only a very enthusiastic belief in

the scope of reciprocity could explain the broad social integration in larger groups
of weakly related humans.
In the 1970s, Alexander had already seen the problem. Primitive human groups
were perhaps something like chimpanzee troops, in which kin selection and reci-
procity could be at least roughly matched to the level of cooperation and social
integration. But human history has been characterized by a great expansion in
group size. How could one account for the transitions from chimpanzee troop to
village to nation-state? Group against group competition potentially explains the
benefit of larger group size. But what prevented internal conflict in larger groups,
which could no longer be bound by close relatedness or tight reciprocity?
Without some mechanism to control those internal conflicts, larger groups
could not be sustained. Stating the puzzle in that way, the solution is clear. There
must be some mechanism that suppresses internal conflict. If individuals cannot
compete against members of their own group, then they can only increase their
success by increasing the success of the group as whole. Suppression of internal
competition unites all group members into a cohesive and cooperative unit.
That idea of internal suppression and group cohesion is the new theory of
cooperation that I took away from The Biology of Moral Systems. I was truly sur-
prised that so simple and so powerful an explanation could appear as a new idea
in 1987. For Alexander, human moral systems were systems for regulating internal
competition within groups to promote group cohesion and success in competition
against other groups. The broader generality of regulating internal competition
in biological evolution was clear to Alexander, and he had in fact reasoned about
human evolution by extension of his understanding of the evolutionary history
of life.
Of course, no truly deep and general idea appears out of nothing. The first
clear description often coincides with others who soon express similar notions
arising out of independent lines of study. In the early 1990s, I became increasingly
interested in Alexander’s theory of internal suppression as a way to achieve group
integration. My own interest developed because I was trying to understand the
principles by which early genomes arose near the origin of life. How did differ-
ent replicating molecules come together to form larger, cohesive genetic systems?
I felt that was an important question, because it seemed that we could not say we
understood any aspect of sociality if we could not at least give a plausible theory
for the origin of genomes.
The more I thought about it, the more I realized that, at that time in the early
1990s, we really did not have the conceptual tools to give a plausible theory of
the origin of genomes. So I was brought back to Alexander’s vision of how bio-
logical systems could achieve broader group integration in spite of limited related-
ness and limited opportunities for reciprocity and synergism. Specifically, I had
to understand how a theory of suppression of internal competition could work
broadly in evolutionary theory.
42 { General Foundations

In effect, I needed to work out the step-by-step aspects of Alexander’s theory

applied to the origin of genomes, in the absence of any advanced behavioral or
cognitive abilities. My own work appeared in Frank 1995, but that is not the key
point here. What matters is that I also had to understand the historical genesis of
Alexander’s thinking and the different parallel lines by which similar ideas devel-
oped through the 1980s and 1990s (Frank 2003).
Alexander cited two clear precedents to his own ideas. First, John Rawls’s (1971)
famous theory of justice from moral philosophy developed the notion of the “veil
of ignorance.” A just society establishes rules that individuals regard as fair from
behind a veil of ignorance about their position within society. An individual may,
in practice, end up on one end or the other of any particular social interaction.
(Harsanyi [1953] developed a similar idea; see Skyrms [1996] for discussion of
these ideas in an evolutionary context.)
It does not pay to argue the fine details of how precisely these humanistic
thoughts presage current evolutionary understanding. These thoughts from moral
philosophy do contain the following kernels: group cohesion returns benefits to
individuals, and randomization of position levels individual opportunity and pro-
motes group cohesion. In other words, given randomization of individual success
within the group, an individual increases success only by increasing the success of
the group as a whole.
The second precedent came from Leigh’s (1971, 1977) work on Mendelian seg-
regation in meiosis. In standard diploid genetics, each genetic locus has one allele
from the mother and one from the father. Each gamete made by an individual
has either the maternal or paternal allele. Mendelian segregation, or fair meiosis,
gives an equal chance to maternal and paternal alleles of being in a successful
gamete. Meiotic drive subverts fairness by giving one allele a greater chance of
transmission. The pieces of chromosomes that can drive against their partners
gain a reproductive advantage by increasing their chance for transmission to off-
spring. As driving chromosomes spread because of their transmission advantage,
they often carry along deleterious effects that are partly protected from selection
by being associated with transmission advantage (Zimmering et al. 1970).
Other parts of the genome lose when a driving chromosome carries with it
deleterious effects into the majority of gametes. Suppression of drive has the
immediate effect of reducing association with the deleterious effects of driving
chromosomes; it has the long-term consequence of taking away the transmission
advantage that protects the deleterious effects. Drive suppression thus helps to
purge the genome of the deleterious effects carried by driving chromosomes. The
many genes of the genome repress the drive ‘‘as if we had to do with a parliament
of genes, which so regulated itself as to prevent ‘cabals of a few’ conspiring for their
own ‘selfish profit’ at the expense of the ‘commonwealth’’’ (Leigh 1977, p. 4543).
When meiosis is fair, randomization puts each allele behind a veil of ignorance
with regard to its direct transmission (interests) in each progeny. Behind the veil,
each part of the genome can increase its own success only by enhancing the total
 Cooperation } 43

number of progeny and thus increasing the success of the group. However, dis-
cussing ‘‘interests’’ in arguments about how natural selection operates can be mis-
leading. In this case, natural selection directly favors the immediate advantage of
drive suppression, which reduces association with the deleterious effects that often
hitchhike along with drive. The long-term advantage of purging the hitchhiked
deleterious effects also contributes to favoring drive suppression when groups
compete against groups, for example, species against species (Leigh 1977).
Leigh (1977) noted that alignment of individual and group interests shifts selec-
tion to the group level. However, meiosis was the only compelling case known at
that time. Without further examples, there was no reason to emphasize repression
of internal competition as an important force in social evolution and the forma-
tion of evolutionary units. From the conceptual point of view, it may have been
clear that repression of internal competition could be important, but not clear how
natural selection would favor such internal repression.
Alexander and Borgia (1978) joined Leigh in promoting the possible great
potency of internal repression in shaping interests and conflicts in the hierarchy
of life. From this, Alexander (1979, 1987) developed his theories of human social
structure (see introductory quotes). In this theory, intense group-against-group
competition shaped societies according to their group efficiencies in conflicts.
Efficiency, best achieved by aligning the interests of the individual with the group,
favored in the most successful group’s laws that partially restricted the opportuni-
ties for reproductive dominance within groups. For example, Alexander (1987)
argued that socially imposed monogamy levels reproductive opportunities, partic-
ularly among young men at the age of maximal sexual competition. These young
men are the most competitive and divisive individuals within societies and are the
pool of warriors on which the group depends for its protection and expansion.
If these young men cannot compete against their neighbors within their groups,
then they can increase their success only by cooperating with their neighbors in
competition against other groups.
Rawls and Leigh directly influenced Alexander. With regard to biology, Leigh
(1971, 1977) may have been the first to emphasize how repression of internal com-
petition aligns individual and group interests. However, meiosis provided the only
good example at that time, so the idea did not lead immediately to new insight.
Alexander (1979, 1987) used Leigh’s interpretation of meiosis as the foundation
for his novel theories about human social evolution. I was aware of the discussion
about meiosis in the 1970s, but I only realized the general implications for repres-
sion of competition as a powerful evolutionary force after reading Alexander
(1987). With two examples—meiosis and the structuring of social groups—I could
see how a simple idea could be applied to different contexts.
Around the same time, Buss (1987) was independently analyzing cellular com-
petition in metazoans. Many multicellular animals are differentiated into tissues
that predominantly contribute to gametes and tissues that are primarily nonrepro-
ductive. This germ-soma distinction creates the potential for reproductive conflict
44 { General Foundations

when cells are not genetically identical. Genetically distinct cellular lineages can
raise their fitness by gaining preferential access to the germline. This biasing can
increase in frequency even if it partly reduces the overall success of the group.
One way to control renegade cell lineages is to enforce a germ-soma split early
in development (Buss 1987). This split prevents reproductive bias between lineages
during subsequent development. Once the potential for bias has been restricted, a
cell lineage can improve its own fitness only by increasing the fitness of the indi-
vidual. This is another example of how reproductive fairness acts as an integrating
force in the formation of units.
Buss stimulated Maynard Smith (1988) to consider how social groups became
integrated over evolutionary history. Maynard Smith disagreed with Buss’s partic-
ular argument about the importance of the germ-soma separation in metazoans.
But in considering the general issues, Maynard Smith had in hand several possible
examples of group integration, including meiosis and genomic integration and
perhaps repression of cellular competition in metazoans. From these examples,
Maynard Smith (1988, pp. 229-230) restated the essential concept in a concise and
very general way:

One can recognize in the evolution of life several revolutions in the way in
which genetic information is organized. In each of these revolutions, there
has been a conflict between selection at several levels. The achievement of
individuality at the higher level has required that the disruptive effects of
selection at the lower level be suppressed.

This view led to Maynard Smith and Szathmary’s (1995) book The Major Transitions
in Evolution, a popular account of the history of life based on the key events in which
competition within groups became suppressed. Maynard Smith and Szathmary’s
synthesis arose independently from Alexander’s work. But Alexander was the first
to take Leigh’s insight about meiosis and apply that view in a general and power-
ful way to propose a solution to the puzzle of progressive social integration of
complex groups. Buss (1987) came soon after. In this light, The Major Transitions
in Evolution can be seen as the great development and synthesis of Alexander’s
insight about suppression of competition in the evolution of cooperation.
Since 1995, suppression of competition has developed into a broad research
topic applied to many puzzles of cooperative evolution. I list just three of the most
recent applications taken from articles published during the past few years. These
applications give a sense of the research that has grown out of Alexander’s original
insights. Frank (2003) reviews several additional examples.
Higginson and Pitnick (2011) summarize aspects of competition between
sperm within the ejaculate of a single male. They conclude by noting the potential
importance of mechanisms that repress such intra-ejaculate competition (p. 265):

Competition between sibling sperm may reduce male reproduc-

tive fitness, even in monogamous systems, by reducing the number of
 Cooperation } 45

fertilization-competent sperm per ejaculate (e.g. killing of Y-chromosome-

bearing sperm in the case of sex chromosome meiotic drive) or by dis-
placing sibling sperm from the site of storage or fertilization. Male-level
selection for adaptations that reduce intra-ejaculate competition in favour
of improved whole-ejaculate success aligns the interests of males and the
sperm they produce. When competition between sibling sperm is restricted
or prevented, individual sperm fitness can only be maximized by enhancing
inter-ejaculate competitive success (Frank 2003). We refer interested readers
to two recent reviews for a more detailed discussion of sperm-level selection
and male-sperm conflict (Immler 2008; Pizzari and Foster 2008).

Hoffmann and Korb (2011) studied replacement of reproductives in termite colo-

nies. They emphasized the potential importance of mechanisms that repress com-
petition during the replacement phase of the colony life cycle. They noted “Strong
conflicts were predicted as all colony members (except soldiers) have the capa-
bility to become neotenic replacement reproductives. Our behavioural observa-
tions first implied that there was no overt conflict during replacement, but the
killing of some neotenics suggested that conflict was not completely suppressed.
Various mechanisms were found that may regulate conflict” (p. 270). Among pos-
sible mechanisms that may repress competition in the colony, they emphasize a
possible form of randomization analogous to fair meiosis:
One proximate mechanism that can reduce overt conflict is the sensitive
period: a short period during the moulting interval when the developmental
fate of an organism at the next moult is determined. . . . During this period,
individuals are sensitive to environmental stimuli, such as the absence of
reproductives. . . . Among the workers, only individuals in the sensitive
period are able to respond to orphaning and become neotenic replacement
reproductives. As all workers regularly pass through this period, they all
have a fair chance of becoming neotenic, while at the same time the num-
ber of actually competing individuals is reduced. Thus, the sensitive period
functions as a ”fair lottery” mechanism similar to, for example, Mendelian
segregation during gamete formation (Frank 2003).
The evidence remains ambiguous with respect to this argument for a fair lottery
mechanism to repress competition. The point here is that Alexander’s conceptual
framing of cooperative evolution plays a key role in Hoffman and Korb’s (2011)
thinking about termite biology.
Many other aspects of social insect cooperation have been interpreted with
respect to repression of competition within colonies (Ratnieks et al. 2006). Smith
et al.’s (2009) recent study continues the development of this topic. They summa-
rize their conclusions (p. 78):

Cheaters are a threat to every society and therefore societies have estab-
lished rules to punish these individuals in order to stabilize their social
46 { General Foundations

system. . . . Recent models and observations suggest that enforcement of

reproductive altruism (policing) in hymenopteran insect societies is a
major force in maintaining high levels of cooperation. . . . In order to be
able to enforce altruism, reproductive cheaters need to be reliably identi-
fied. . . . [Our data provide] the first direct evidence that cuticular hydro-
carbons are the informational basis of policing behaviors, serving a major
function in the regulation of reproduction in social insects. We suggest that
even though cheaters would gain from suppressing these profiles, they are
prevented from doing so through the mechanisms of hydrocarbon biosyn-
thesis and its relation to reproductive physiology. Cheaters are identified
through information that is inherently reliable.
The current literature contains many additional applications of Alexander’s theory
of cooperative evolution. Repression of competition has indeed joined kin selec-
tion as the second key process in the major evolutionarily transitions throughout
the history of life.

Acknowledgments

Parts of this introduction were taken from Frank (2003). My research is supported
by National Science Foundation grant EF-0822399, National Institute of General
Medical Sciences MIDAS Program Grant U01-GM-76499, and a grant from the
James S. McDonnell Foundation.

References
Alexander, R.D. 1979. Darwinism and Human Affairs. Seattle: University of Washington
Press.
Alexander, R.D. 1987. The Biology of Moral Systems. New York: Aldine de Gruyter.
Alexander, R.D. 2011. The Mockingbird’s River Song: Poems, Essays, Songs and Stories,
1946-2011. Manchester, MI: Woodlane Farm Books.
Alexander, R.D., and Borgia, G. 1978. Group selection, altruism, and the levels of organiza-
tion of life. Annu. Rev. Ecol. Syst. 9:449–474.
Buss, L.W. 1987. The Evolution of Individuality. Princeton, NJ: Princeton University Press.
Frank, S.A. 1995. Mutual policing and repression of competition in the evolution of coop-
erative groups. Nature 377:520–522.
Frank, S.A. 2003. Repression of competition and the evolution of cooperation. Evolution
57:693–705.
Harsanyi, J. 1953. Cardinal utility in welfare economics and the theory of risk taking. J. Pol.
Econ. 61:434–435.
Higginson, D.M. and Pitnick, S. 2011. Evolution of intra-ejaculate sperm interactions: do
sperm cooperate? Biol. Rev. 86:249–270.
Hoffman, K. and Korb, J. 2011. Is there competition over direct reproduction in lower ter-
mite colonies? Anim. Behav. 81:265–274.
 Cooperation } 47

Immler, S. 2008. Sperm competition and sperm cooperation: the potential role of diploid
and haploid expression. Reproduction 135:275–283.
Leigh, E.G., Jr. 1971. Adaptation and Diversity. San Francisco: Freeman, Cooper.
Leigh, E.G., Jr. 1977. How does selection reconcile individual advantage with the good of the
group? Proc. Natl. Acad. Sci. USA 74:4542–4546.
Maynard Smith, J. 1988. Evolutionary progress and levels of selection. In: M.H. Nitecki
(ed.), Evolutionary Progress. Chicago: University of Chicago Press.
Maynard Smith, J., and Szathmary, E. 1995. The Major Transitions in Evolution. San Francisco:
Freeman.
Pizzari, T. and Foster, K. 2008. Sperm sociality: Cooperation, altruism, and spite. PLoS
Biol. 6, e130.
Ratnieks, F.L.W., Foster, K.R., and Wenseleers, T. 2006. Conflict resolution in insect societ-
ies. Annu. Rev. Entomol. 51:581–608.
Rawls, J. 1971. A Theory of Justice. Cambridge: Harvard University Press.
Skyrms, B. 1996. Evolution of the Social Contract. Cambridge: Cambridge University Press.
Smith, A.A., Holldobler, B., and Liebig, J. 2009. Cuticular hydrocarbons reliably identify
cheaters and allow enforcement of altruism in a social insect. Current Biology 19:78–81.
West-Eberhard, M.J. 1975. The evolution of social behavior by kin selection. Q. Rev. Biol.
50:1–32.
Zimmering, S., Sandler, L. and Nicoletti, B. 1970. Mechanisms of meiotic drive. Annu. Rev.
Genet. 4:409–436.
 HUMANS

Ultrasociality Based on Reciprocity

Excerpt from: Alexander, R. D. 1986. The Biology of Moral Systems. New York,
Aldine Press.

Humans have taken a route to ultrasociality entirely different from that of the
social insects. In the largest and evidently most unified or stable human groups
(i.e., large, long-lasting nations) partial (rather than complete) restrictions on
reproduction have the effect of leveling or equalizing opportunities to reproduce.
Socially imposed monogamy and graduated income taxes are examples of such
reproductive opportunity leveling. The tendency in the development of the largest
human groups, although not always consistent, seems to be toward equality of
opportunity for every individual to reproduce via its own offspring, rather than
toward specializing baby production in one or a few individuals and baby care in
the others. However humans specialize and divide labor, they nearly always insist
individually on the right to carry out all of the reproductive activities themselves.
One consequence is that the human individual has evolved to be extraordinarily
complex (and evidently to revere individuality), and another is that the complex-
ity and variety of social interactions among human individuals is without parallel.
Because human social groups are not enormous nuclear families, like social insect
colonies, a third consequence is that competition and conflicts of interest are also
diverse and complex to an unparalleled degree. Hence, I believe, derives our topic
of moral systems. We can ask legitimately whether or not the trend toward greater
leveling of reproductive opportunities in the largest, most stable human groups
indicates that such groups (nations) are the most difficult to hold together without
the promise or reality of equality of opportunity (see also Alexander 1974, 1979a;
Alexander and Noonan, 1979; Strate, 1982; Betzig 1986).

Other Special Cases of Cooperation

GENES IN GENOMES
A corollary to reproductive opportunity leveling in humans may occur through
mitosis and meiosis in sexual organisms. It has generally been overlooked that
these very widely studied processes are so designed as usually to give each gene
 Cooperation } 49

or other genetic subunit of the genome (= the genotype or set of genetic materials
of the individual) the same opportunity as any other of appearing in the daugh-
ter cells. Alexander and Borgia (1978) and Williams (1979) have speculated that
this equality of opportunity came about because only alleles with equal (or better)
likelihoods of being present in daughter cells have survived; possibly, more gener-
alized mechanisms have come to be involved in modern forms. It is not inappro-
priate to speculate that the leveling of reproductive opportunity for intragenomic
components—regardless of its mechanism—is a prerequisite for the remarkable
unity of genomes, some of them composed of thousands or hundreds of thousands
of recombining, potentially independent genes and other subunits (Leigh, 1983;
Alexander and Borgia, 1978).

MONOGAMOUS PAIRS
To the extent that males and females (of any species) commit themselves to life-
time monogamy, the interests of two individuals in a pair approach being iden-
tical. This point is often confused by biologists and social scientists alike (e.g.,
Dawkins, 1976, and Sahlins, 1976, both thought that unrelated spouses necessar-
ily disagree more than relatives). The reason is the same as that causing iden-
tity of interests in the different individual workers in a eusocial insect colony:
the two different individuals realize their reproduction through identical third
parties which each of them gain by helping a great deal. In the case of worker
insects the third parties are the reproductive brothers and sisters produced by
the queen, their mother. If the queen dies and is replaced by one of the work-
ers’ siblings, the situation may not be altered even though the workers are less
closely related to a sister’s offspring than to their sisters, and less closely related
to a sister’s offspring than is the sister herself. When a queen changeover occurs,
unless workers retain some ability and likelihood of themselves becoming the
queen (and in many modern species they have lost this ability), they can do
no better than by cooperating fully with one another to produce reproductive
nieces and nephews.
Given that the members of monogamous pairs are evolved to invest parentally,
then, to the extent that (1) philandering is unlikely or too expensive to be profit-
able, and (2) the relatives of one or the other are not significantly more available
for nepotistic diversions of resources, each member of the pair will profit from
complete cooperation with the other to produce and rear their joint offspring. In
humans this condition is most likely in (1) societies in which (a) families live and
work separately and (b) husband and wife are in fairly close contact most of the
time and (2) societies in which married couples are “neolocal,” living in some new
location apart from both sets of relatives but close enough to be affected by the
interests of their kin networks in sustaining the marriage. In such societies (which
historically have probably been most often agricultural), I predict that the devo-
tion of husband and wife will be measurably most complete.
50 { General Foundations

Aside from clones, social insects and humans have developed the largest known
societies, measured by numbers of complexly interacting individuals. They are
also the most complexly communicating organisms. They have both accomplished
this by expanding confluences of interest and reducing conflicts of interests, and it
is at least possible that monogamy was involved in both cases, early in the evolu-
tion of social insects and late in the evolution of the largest human societies. What
we have to understand, for both social insects and humans, is how the situations
develop in which workership and monogamy, respectively, come to be the rule
or norm. I believe I am correct in saying that in neither case are the answers yet
available.

Monogamy and Reproductive Opportunity Leveling

Our understanding of the manner in which monogamous pairs come to coop-

erate is not much better than our understanding of why social insect colonies
sometimes become huge and sometimes do not. Because monogamy in large
technological nations is imposed socially (meaning that the costs of its alter-
natives are imposed by the rest—or some part—of society), understanding its
background becomes a part of the effort to understand moral systems. Alexander
et al. (1979; see also Alexander, 1975) have argued that socially or legally imposed
monogamy is a way of leveling the reproductive opportunities of men, thereby
reducing their competitiveness and increasing their likelihood of cooperative-
ness. The imposition of monogamy by custom or law has the interesting effect
of reducing both male-male and male-female conflicts to a minimum, especially
when clans are discouraged (as in nation states: see Alexander, 1979a, pp. 256-
259), and when married couples do not have differential access to their respective
relatives (e.g., when they are “neolocal” or reside in a new locality rather than
becoming a part of one or the other extended family of relatives). Moreover, the
combination of socially or legally imposed monogamy, neolocality, and close
association of the married couple in work not only leads to minimizing of phi-
landering and conflict of interest between husband and wife, but also character-
izes the largest (and perhaps the most unified—or durable—of all large) human
societies. Young men at the age of maximal sexual competition are the most divi-
sive and competitive class of individuals in human social groups; they are also
the pool of warriors. It is not trivial that socially imposed monogamy (and the
concomitant discouragement of clans as extended families that control mem-
bers) correlates with (1) justice touted as equality of opportunity; (2) the concept
of a single, impartial god for all people; and (3) large, cohesive, modern nations
that wage wars and conduct defense with their pools of young men (Alexander,
1979a). To a large extent socially imposed monogamy has spread around the
world by conquest. The social imposition of monogamy thus simultaneously
(1) inhibits the generation of certain kinds of within-group power dynasties that
 Cooperation } 51

might compete with government and lead to divisive within-group competi-

tion and (2) promotes those activities and attitudes that generate and maintain
success in the wielding of reciprocity as the binding cement of social structure
(honesty, sincerity, trust).
Humans almost certainly began to evolve their social tendencies and capabili-
ties in small kin groups. If so, during that process they incidentally acquired the
capability to maintain social organization in ever larger and more complex social
groups through systems of reciprocity rather than nepotism per se. In such groups
there is only one way to approach an equalization of reproductive opportunity, and
that is by sets of rules or moral systems. In humans the laws and mores of larger
and larger groups seem increasingly to (1) guarantee to every individual the right
to produce and rear its own offspring and (2) restrict the amount and likelihood of
variation in reproduction among families. China is currently an extreme in both
size (over one billion) and regulation of reproduction (Keyfitz, 1984). Until 1981 or
1982, government assistance was given for a first child, but funds were withdrawn
if a second was born. More recently it was reported (e.g., Ann Arbor, Michigan,
News, 1982; “Nova” and “60 Minutes” television programs, 1984) that enormous
pressure for sterilization followed the birth of a single child. Not long ago, India
briefly attempted to require sterilization after three children were born to any per-
son; the government of India now pays individuals who submit to sterilization.
More subtle, but also more widespread, are laws that reduce variance in access to
resources, such as graduated income taxes, the vote, representative government,
elected (not hereditarily succeeding) officials, and universal education.
MacDonald (1983) discusses the “leveling” effect of monogamy, although he
seems to find it puzzling, in evolutionary terms, perhaps because he does not con-
sider the significance of equality of opportunity as a basis for social unity in the
face of extrinsic threats. Once this factor is weighed in, one sees that the real puzzle
is not, as MacDonald supposes, to account for leveling processes, but to account
for the maintenance of despotic societies, within which the greatest disparities in
opportunities for individuals occur (e.g., Betzig, 1986); or, rather, to explain why
some sizes and kinds of societies involved huge disparities in individual opportu-
nity (those intermediate in size; Alexander, 1979a), while others (large and small)
have leveled them to extreme degrees. I think the answer will come from compar-
ing the histories of interaction between neighboring societies, effects of physical
or physiographic barriers on their sizes, and separation of warriors (soldiers) from
their families.
Despite their obvious and dramatic differences from one another, then, the most
extremely ultrasocial systems of humans and other species are apparently all based
on reproductive opportunity leveling. The essential difference is that in (some)
clones and eusocial forms all individuals realize their reproduction through the
same sets of babies and have specialized baby production and baby care in differ-
ent individuals, and humans have done neither of these things.
52 { General Foundations

Literature Cited

Alexander, R.D. 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5:352–383.
Alexander, R.D. 1975. The search for a general theory of behavior. Behav. Sci. 20: 77–100.
Alexander, R.D. 1979a. Darwinism and Human Affairs. Seattle: University of Washington
Press.
Alexander, R.D. and G. Borgia. 1978. On the origin and basis of the male-female phenom-
enon. In Sexual selection and reproductive competition in insects, M. F. Blum and N. A.
Blum (eds.). Academic Press, pp. 417–440.
Alexander, R.D., J.L. Hoogland, R.D. Howard, K.L. Noonan, and P.W. Sherman. 1979.
Sexual dimorphism and breeding systems in pinnipeds, ungulates, and humans. In
Evolutionary Biology and Human Social Behavior: An Anthropological Perspective, N.A.
Chagnon and W. G. Irons (eds.). North Scituate, Mass.: Duxbury Press, pp. 402–435.
Alexander, R.D. and K.L. Noonan. 1979. Concealment of ovulation, parental care and
human social evolution. In Evolutionary Biology and Human Social Behavior: An
Anthropological Perspective, N. A. Chagnon and W. G. Irons (eds.). North Scituate,
Mass.: Duxbury Press, pp. 436–453.
Betzig, L. 1986. Despotism and differential reproduction: A Darwinian view of history.
Hawthorne, N.Y.: Aldine.
Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press.
Keyfitz, N. 1984. The population of China. Sci. Amer. 250:38–47.
Leigh, E.G. 1983. When does the good of the group override the advantage of the indi-
vidual? Proc. Natl. Acad. Sci. U.S. 74:2985–89.
MacDonald, K. 1983. Population, social controls and ideology: Toward a sociobiology of the
phenotype. J. Social Biol. Struct. 6:297–317.
Sahlins, M.D. 1976. The Use and Abuse of Biology: An Anthropological Critique of Sociobiology.
Ann Arbor, : University of Michigan Press.
Strate, J.M. 1982. An evolutionary view of political culture. Ph.D. dissertation, University
of Michigan.
Williams, G.C. 1979. The question of adaptive sex ratio in outcrossed vertebrates. Proc.
Royal Soc. London B 205:567–580.
3}

Eusociality in Naked Mole-Rats

Heroes Are Works of Art

Inspirations decorating the walls of minds,
invitations to previously impossible reaches,
barely glimpsed peaks of uniqueness,
standouts in endless seas of possibilities.
Heroes stretch the imagination,
promising itineraries of unfolding expansion;
they proffer guides to the triumphs of synthesis,
declare the meaning of life.
Heroes model reality and security, sanction
scenarios, activate and reactivate those
billions of our cortical neurons said to be
of hundreds of kinds, enabling their million
billions of connections comprising the most
elaborately complex and precious machinery
conceivable anywhere
any time
yet.
***
Heroes are for all times, all ages
they help us to know what we
hadn’t even known we wanted to know,
to facilitate all that we discover
can be discovered, all that
can be absorbed into ourselves.
Alexander 2011, p. 52
This page intentionally left blank
 INTRODUCTION

Richard Alexander, the Naked Mole-Rat, and the

Evolution of Eusociality
Paul W. Sherman

Eusociality is an entomologically derived term that identifies animal social systems

with three characteristics: (1) multigenerational groups, (2) alloparental care of
young (helpers), and (3) restriction of reproduction to a fraction of the individuals
in each group (i.e., reproductive “skew”). Eusociality has been an important evo-
lutionary puzzle ever since Darwin (1859: 268) highlighted worker ants as present-
ing “one special difficulty which at first appeared to me insuperable, and actually
fatal to the whole theory.” Because natural selection favors increased reproduction,
how can individuals evolve gradually to reproduce less and less or not at all? And
how can specialized morphological, physiological, and behavioral characteristics,
including spectacular acts of suicidal altruism, evolve among individuals that do
not directly reproduce?
Until the late 1970s eusociality was thought to occur only in two orders
of insects: the Hymenoptera (ants, bees, and wasps) and the Isoptera (ter-
mites). Then in 1981 Jennifer Jarvis announced the discovery of eusociality in
a mammal, the naked mole-rat (Heterocephalus glaber, order Rodentia, fam-
ily Bathyergidae; Jarvis 1981). This was a watershed event in studies of social
evolution, and Richard Alexander played a pivotal role. Several years previ-
ously Alexander had started thinking seriously about the evolution of eusocial-
ity. Contrary to prevailing wisdom at the time, Alexander believed the ecological
factors that favored extended maternal care of offspring and natal philopatry,
especially predation and limitation of suitable nest sites, were more important
than extraordinarily close genetic relatedness between helpers and beneficiaries
in predisposing organisms to eusociality. Accordingly, he hypothesized an imagi-
nary eusocial mammal that lived like a termite in a safe, expandable tunnel system
deep underground in rock-hard soil, where it fed on subterranean plant parts.
Alexander presented his ideas in professional seminars and after one of these a
colleague told him that his hypothetical mammal sounded a lot like the naked
mole-rat of eastern Africa.
Alexander was astonished—and energized. He corresponded with Jarvis, then
the world’s naked mole-rat expert, and in the fall of 1979 he and I and our spouses
visited her at the University of Cape Town in South Africa. We will never forget
56 { General Foundations

the thrill of entering Jarvis’s laboratory and seeing those remarkable little furless,
buck-toothed rodents scurrying through yellow plastic tunnel systems backward
and forward, head-to-tail, like tube trains. A round box served as a nest, and col-
ony members congregated there, snuggling together in a jumbled pile atop which
sprawled a particularly large, elongate individual: the queen (breeding female).
Instantly we realized that before us was the connection between vertebrate and
invertebrate social systems—a new clue to understanding the puzzle of eusociality!
Soon after our arrival, Jarvis presented Alexander and me with a draft of her
now famous 1981 Science paper. We commented extensively on it, and a friendship
born in shared excitement and scientific curiosity quickly developed. We invited
Jarvis to join our expedition to Kenya the following week. She agreed and, work-
ing together, we collected six partial colonies of naked mole-rats near Mtito Andei,
a little village 233 km southeast of Nairobi. These animals were sent to Cornell
University and the University of Michigan for studies of the animals’ social and
reproductive behaviors.
Results of the first decade of mole-rat research were summarized in a book
entitled The Biology of the Naked Mole-Rat (Sherman et al. 1991). The excerpt that
follows is from the book’s first chapter, which Alexander had begun writing some
15 years previously. The chapter is comprehensive, and too long to be included in
its entirety in this volume. However, the portions that had to be omitted contain
important insights and arguments and, to place the reprinted excerpt in context,
I will highlight several of these.
First, Alexander et al. (1991) noted that because naked mole-rats and termites
are diploid, their social systems confirm W. D. Hamilton’s (1964) original argu-
ment that although close relatedness facilitates the evolution of altruism, haplo-
diploidy is neither necessary nor sufficient to account for eusociality. However,
failure of the specific “¾ relatedness hypothesis” does not cast doubt on the
importance of kin selection in the evolution of eusociality (West-Eberhard
1975; Queller & Strassmann 1998; Foster et al. 2006; Abbot et al. 2011), contrary
to some recent assertions (e.g., Wilson 2005, 2008; Nowak et al. 2010). Instead,
it suggests that factors in addition to kinship were evolutionary antecedents of
eusociality. Alexander et al. argued that extended maternal care of offspring
requiring progressive food provisioning (“subsociality” in entomological jar-
gon) and incomplete metamorphosis (no pupal stage between immature and
adult) were the key prerequisites in termites and mole-rats. Andersson (1984)
came to similar conclusions in another important paper on the evolution of
eusociality that was being developed at roughly the same time as Alexander’s
manuscript.
Second, Alexander et al. (1991) noted that naked mole-rats prove eusociality is
not unique to insects, refuting explanations that hinge on peculiarities of insect
physiology, genetics, or evolutionary history. Indeed eusociality has now been
discovered in a diversity of organisms including other African mole-rats (Jarvis
et al. 1994; Wallace and Bennett 1998), another class of invertebrates (Crustacea:
 Eusociality in Naked Mole-Rats } 57

sponge-dwelling shrimp [Duffy et al. 2000]), and other orders of insects, some of
which are haplodiploid (e.g., Hemiptera: gall-nesting thrips [Crespi et al. 1997])
but others not (Coleoptera: ambrosia beetles [Kent and Simpson 1992; Smith
et al. 2009]; Homoptera: gall-forming aphids [Stern and Foster 1996]). These con-
vergences raise the question: what common selective pressures favored eusociality
in such phylogenetically and physiologically divergent creatures?
Third, Alexander et al. (1991) used the naked mole-rat to draw parallels
between social evolution in vertebrates and invertebrates. Cooperative breed-
ing and eusociality occur in birds, mammals, arthropods, and a few fishes when
ecological pressures preclude independent dispersal and reproduction, groups
cooperate to forage and defend themselves, and individuals can raise their inclu-
sive fitness sufficiently by rearing siblings to compensate for foregoing personal
reproduction (see also Andersson 1984). Thus both “extrinsic” (ecological) and
“intrinsic” (genetic and developmental) factors are important in favoring coop-
erative breeding and eusociality (Evans 1977). The significance of both types of
factors is captured in Hamilton’s Rule, which posits that altruistic acts are favored
by natural selection when rB – C > 0, where “C” is the personal fitness cost to
the altruist, “B” is the fitness benefit to the recipient, and “r” is the relatedness
between them.
Among the extrinsic factors, Alexander et al. (1991) believed that protection
from predation was paramount. They argued that the evolution of eusociality
was facilitated by availability of safe, long-lasting, expansible nest sites. Such “for-
tresses” (Queller and Strassmann 1998) would have to be defensible by small num-
bers of armed individuals (e.g., possessing potent stings, chemical weaponry, or
sharp teeth), expandable to accommodate the growing family, and surrounded by
sufficient food resources to feed the entire group. All are true for naked mole-rats
(Brett 1991) and single-site nesting termites (Shellman-Reeve 1997). Among the
intrinsic factors, kinship is essential because all cooperatively breeding and euso-
cial species live in family groups. Ancestrally, most of these were monogamous
(for social insects, see Hughes et al. 2008; for birds, see Cornwallis et al. 2010) so
recipients of help usually were full siblings.
The behavior of a young helper mole-rat or termite conforms to Hamilton’s
Rule because the cost to the helper (C) for staying in the safety of the natal burrow
system is low since risks of independent dispersal are substantial; the benefit (B) to
younger siblings is high because food provisioning by helpers promotes their rapid
growth and helpers’ fortress defense behaviors effectively protect them from pred-
ators; and relatedness (r) is high because helpers and recipients typically are full
siblings, with inbreeding increasing their relatedness more (for naked mole-rats,
see Reeve et al. 1990; for subterranean termites, see Vargo and Husseneder 2009).
Developmental factors also are important because a helper can begin enhancing
its inclusive fitness long before reaching adult size, thereby gaining a head start in
reproduction (and therefore senescence) over individuals that wait until they are
large and old enough to rear their own offspring. Queller (1989) was stimulated
58 { General Foundations

by Alexander’s eusociality manuscript to expand the latter idea to cases where the
reproductive head start occurs because helpers can rapidly bring juvenile siblings
to independence.
One question that Alexander et al. (1991) sidestepped was whether coopera-
tively breeding species with helpers that differ morphologically and behaviorally
from breeders (i.e., a worker “caste”) are qualitatively different from species in
which helpers and breeders are similar morphologically and equally totipotent.
The issue is important for deciding whether cooperative breeding and eusociality
should be lumped together (Sherman et al. 1995, Hardisty and Cassill 2010) or split
(Crespi and Yanega 1995) theoretically and terminologically. Both proposals have
been endorsed but consensus has not been achieved (Lacey and Sherman 2005,
Beekman et al. 2006), probably because each approach is useful for addressing
questions on different levels of analysis (Sherman 1988). Lumping focuses on simi-
larities in personal reproduction among taxa and facilitates ultimate analyses (i.e.,
evolutionary history and fitness levels) of variations in social structures, whereas
splitting focuses on behavioral and morphological specializations and facilitates
proximate analyses (mechanistic and ontogenetic levels) of reproductive differ-
ences among individuals.
The last section of Alexander et al.’s (1991) excerpt implies that coopera-
tive breeding and eusociality form a continuum of fundamentally similar social
systems whose main differences lie in group sizes and degrees of reproductive
restriction. The evolution of specialized helper phenotypes, loss of behavioral and
reproductive totipotency, and intragroup breeding conflict are related to group
size, which itself is determined by body size and ecological factors (the benefits
of philopatry and costs of attempting to disperse). When organisms are small
and ecological constraints are severe—for example, predation is heavy and safe,
expandable nests sites are limited, or food is patchily distributed and hard to find
but locally abundant in quantity—offspring remain in the natal nest and large
groups form. In such groups the likelihood that any youngster will ever have an
opportunity to breed is vanishingly small, so individuals can transmit their genes
most effectively by focusing on rearing collateral kin. Over evolutionary time this
favors phenotypic specializations that enable helpers to function as super-efficient
food gatherers, food preparers and provisioners, and colony defenders, even at the
expense of loss of reproductive competence.
When body sizes are larger and ecological constraints are less severe the reverse
occurs: Groups are small enough that everyone has a good chance of eventually
breeding so all colony members retain reproductive and behavioral totipotency
and phenotypes do not diverge because the tasks that parents and helpers perform
are similar; the phenotypic plasticity of vertebrates also reduces the likelihood that
alternative morphotypes will evolve. Breeding-age helpers forgo reproduction only
temporarily, so conflicts over breeding are frequent among small-group coopera-
tive breeders (e.g., wolves, wild dogs, meerkats, naked mole-rats, acorn woodpeck-
ers, and paper wasps—see Hart and Monnin 2006; Clutton-Brock 2009), whereas
 Eusociality in Naked Mole-Rats } 59

among large-colony cooperative breeders (most ants and many bees and wasps)
conflict over reproduction is sporadic and occurs primarily over sex allocation
and production of males (Ratnieks et al. 2006).
Cooperative breeding and eusociality thus differ in degree but not in kind.
Classical definitions of eusociality (Hölldobler and Wilson 1990, p. 638) do not
require that some colony members have lost behavioral or reproductive totipo-
tency—only that there is “reproductive division of labor.” Arraying species that
breed cooperatively along a common axis that represents the distribution of life-
time reproductive success (Keller and Perrin 1995) unites studies of vertebrate
and invertebrate societies, and facilitates identification of common extrinsic and
intrinsic selective factors that result in societal convergences. The social struc-
ture of each species results from life-history decisions that are made either over
evolutionary time (for large-group species) or ecological time (for small-group
species—e.g., Tibbetts 2007) about whether or not to disperse from home, attempt
to breed, or help rear siblings (Cahan et al. 2002). At each stage, the evolution-
arily stable decision rule (Darwinian algorithm) is the one that most consistently
results in satisfaction of Hamilton’s Rule.
The book chapter from which the following selection was excerpted is Richard
Alexander’s opus magnum on eusociality. It heightened interest in this social sys-
tem and has steered our thinking about its evolution for the past two decades. In
addition, by highlighting parallels between vertebrate and invertebrate social sys-
tems, Alexander provided a foundation for the recent surge of interest in human
alloparenting (Crittenden and Marlowe 2008; Sear and Mace 2008), cooperative
breeding (Hill and Hurtado 2009; Hrdy 2009; Kramer 2010, 2011), and eusociality
(Foster and Ratnieks 2005; Betzig, 2012). Over the past 20 years, many of the spe-
cific hypotheses presented by Alexander et al. (1991) have been explored and con-
firmed. For example, Bourke (1999) and Anderson and McShea (2001) provided
data that support Alexander et al.’s arguments about how large colony size affects
the evolution of caste differentiation and reproductive conflict in social insects,
Duffy and Macdonald (2010) showed how small body size, natal philopatry, kin-
ship, and availability of safe, expandable nesting sites facilitated the evolution of
eusociality in sponge-dwelling shrimp, and Purcell (2011) confirmed the impor-
tance of predation and food distribution in molding arthropod group sizes and
social organizations.
Since 1991, no paper has been published that treats the evolutionary origins
and adaptive significance of eusociality more comprehensively than Alexander
et al. The most recent review of the evolution of eusociality (Nowak et al. 2010),
although deeply flawed because it dismisses the importance of kin selection (see
Abbot et al. 2011; Rousset and Lion 201; Bourke 2011), nonetheless contains some
good hypotheses about the evolutionary antecedents of eusociality—and all of
them can be found in Alexander et al. (1991). Clearly Alexander et al.’s chapter
has been a guidepost to understanding the evolution of cooperative breeding and
eusociality. It will remain so for many years to come.
60 { General Foundations

Acknowledgments

Thanks to Kyle Summers and Bernie J. Crespi for inviting this contribution, to
Bernie J. Crespi, David C. Queller, Janet Shellman Sherman, and Kyle Summers
for helpful suggestions on the manuscript, and to Richard D. Alexander for
inspiration.

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Tibbetts, E.A. 2007. Dispersal decisions and predispersal behavior in Polistes paper wasp
“workers.” Behav. Ecol. Sociobiol. 61: 1877–1883.
Vargo, E.L. and Husseneder, C. 2009. Biology of subterranean termites: insights from
molecular studies of Reticulitermes and Coptotermes. Annu. Rev. Entomol. 54: 379–403.
Wallace, E.D. and Bennett, N.C. 1998. The colony structure and social organization of the
giant Zambian mole-rat,Cryptomys mechowi. J. Zool. 244: 51–61.
West-Eberhard, M.J. 1975. The evolution of social behavior by kin selection. Q. Rev. Biol.
50: 1–33.
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Wilson, E.O. 2008. One giant leap: how insects achieved altruism and colonial life.
BioScience 58: 17–25.
 THE EVOLUTION OF EUSOCIALITY

Excerpt from R.D. Alexander, K.M. Noonan, B.J. Crespi. The Evolution of
Eusociality. In P.W. Sherman, J.U.M. Jarvis, R.D. Alexander (eds.). The Biology of
the Naked Mole-Rat: 27-32. Princeton, NJ: Princeton University Press.

Safe or Defensible, Long-Lasting, Initially Small,

Expansible, Food-Rich Nest Sites

In addition to gradual metamorphosis, termites and naked mole-rats have the

advantage of a safe niche (microhabitat, nest) from which there is no necessity
to exit because food is abundant within the site and because the niche is both
long-lasting and expansible to accommodate a growing social group. Thus, many
termites live within log fortresses, which are also their food. The nest or niche
expands as the termites excavate the log, and they may also locate additional logs
by burrowing underground and enhance defensibility by thickening or reinforcing
walls with mud. Many species have evolved the ability to construct mud tunnels to
reach additional food sources; some also live underground and forage outside on
grasses (evidently secondarily; Wilson 1971). Naked mole-rats live underground,
feeding primarily on large tubers, which must be approached and located by dig-
ging but which provide continuing food sources that do not require exit from the
relative safety of underground tunnels (see Brett, chap. 5). At least in termites,
nests typically begin small and, in some cases, can be expanded to accommodate
thousands or millions of individuals, with abundant food still available locally.
These conditions are unlike those of virtually all social and solitary (nest-
building) Hymenoptera, which must locate and transport food back to the nest,
often by flying. We suggest that the peculiar combination of nest-site attributes
shared by termites and naked mole-rats represents an important contribution to
the likelihood of their evolving eusociality, compared with the Hymenoptera and
with cooperatively breeding birds and mammals. For the most part, subterranean
mammals either do not have abundant food supplies that can be located and used
without emerging from the safety of the underground tunnels, or their food is
distributed such that, even if they forage underground, the formation and main-
tenance of groups larger than a parent and its offspring are inhibited (e.g., moles
that feed on insects, earthworms, or small subterranean parts of dispersed plants).
Similarly, most birds and nonsubterranean mammals live or nest in locations that
64 { General Foundations

either are not defensible across generations or cannot be expanded to accommo-

date large social groups and still be defensible. A few species, such as hunting
dogs, beavers, dwarf mongooses, and hole-nesting birds, produce offspring in
relative safety and have evolved ways of moving significant amounts of food back
to the den (transport, regurgitation, helper lactation). These are the vertebrate
forms that most closely approach eusocial (see also Lacey and Sherman, chap. 10).
Presumably, if their niches were expansible and their food supplies sufficiently
abundant and localized around the nest site, some of them would have continued
to evolve toward large-colony eusociality.
Four conditions can therefore be postulated that might lead to incipient euso-
ciality. All depend on a safe, maintainable, or improvable (and costly or unlikely)
nest site. (The third condition assumes monogamy and haplodiploidy; the others
assume monogamy but do not require closer relatedness between siblings than
between parent and offspring.)
1. Young are produced faster in the incipient eusocial colony even
though all or virtually all emigrating nonsocial parents find suitable nest
sites and produce viable young. In other words, expanding and improving
a particular kind of nest site after it has been located and started is better
(for the mother, as manipulator, or for the mother and all participating indi-
vidual offspring) than distributing descendants among an adequate number
of nest sites suitable for the raising of a single brood.
2. Young are produced faster in the incipient eusocial colony, but only
because most emigrating nonsocial founders fail to reproduce. In other
words, nest sites (or suitable nest sites) are severely limiting (Emlen 1981,
1984; Koenig and Pitelka 1981).
3. Young are not produced faster or saved in higher proportions in the
incipiently eusocial colonies, but they are more closely related to helpers
than are offspring. Thus, staying home and helping is genetically more prof-
itable than starting a new family if the two alternatives produce the same
number of descendants.
4. Young are not produced faster in the incipiently eusocial colony, but
they are saved and helped enough to cause their producers to outreproduce
noncolonial competitors. In other words, one must imagine that per capita
reproduction becomes increasingly effective with three, four, or even up to
hundreds of thousands of caretakers (parents and alloparents) as compared
with one or two parents.

Nest sites meeting one or more of the above requirements must continue to be
safe for multigenerational periods. If new colonies are initiated by individuals or
pairs, as in most eusocial forms, nest sites may initially be hidden or inconspicuous
or simply not valuable enough as food sources to attract certain kinds of predators.
If eusocial colonies continue to increase in size, however, the nest must become
physically or behaviorally more defensible because larger colonies of organisms
 Eusociality in Naked Mole-Rats } 65

with many juveniles are more attractive and detectable to parasites and predators.
Structural defensibility can be enhanced by extending tunnels and making them
more complex (enabling flight or delaying predators), minimizing sizes and num-
bers of openings into the nest, and enhancing the strength of walls. Behavioral
defensibility can be enhanced by evolving tendencies and abilities of helpers to
ward off attackers and by increasing the numbers of such defenders. Structural and
behavioral defensibility can evolve together as access to a nest is restricted to pas-
sages defensible by individuals or small numbers of individuals (e.g., the enclosed
paper nests of bald-faced hornets) and as individuals evolve increasingly effec-
tive defenses (Wilson 1971) for the particular kinds of structures they defend (e.g.,
enlarged heads and jaws; expellers of toxic substances as in squirt-gun termites,
Nasutitermes). There is a sense here in which eusociality is indeed a continuation
of parental care of offspring hidden or otherwise made safe in a nest.
Most eusocial forms live in the soil. Underground nests can be relatively invul-
nerable and also difficult to locate. Aside from army ant colonies (up to 700,000
individuals), the largest eusocial colonies (ants, termites; up to 10 million) either
live primarily in the soil or extend their nests into it (Wilson 1971). Moreover, most
eusocial forms that maintain nests in the open (primarily wasps) live in the small-
est and least permanent colonies. Their relatives with large colonies (e.g., tropical
wasps, honey bees, and stingless bees) invariably enclose the nest, either in a cav-
ity or an enveloping structure (West-Eberhard, pers. comm.). In addition, they
have evolved the ability to eliminate the small-colony vulnerable stages from their
nesting cycle by swarming to found new colonies, and they are particularly aggres-
sive and feared by humans (and probably other vertebrates). Army ants, which are
nomadic and fearsome even to large vertebrates, also fission to start new colonies.
Fallen tree trunks appear to rank next to soil as nesting sites meeting the above
requirements.
Nesting sites that promote eusociality must also be places where a single female
can monopolize the production of offspring and the use of helpers during the early
stages in the evolution of eusociality. If our scenario emphasizing such origins is
appropriate, these requirements appear to rule out locations, such as caves, where
multiple safe and proximal sites for single-female or pair nesting prevent such
monopolization.
It seems to follow from the argument thus far that small animals are more likely
than large ones to evolve eusociality. We speculate that large animals, such as
birds and mammals, may not be able to increase the value of logs and tree trunks
sufficiently to allow them to evolve eusociality in such places and that nest-site
limitations were thus crucial in such forms. Several predictions about vertebrate
sociality follow. First, the most nearly eusocial vertebrates should be expected to
live in the soil, in large hollow trees or logs, or in constructed dens with similar
characteristics (as do beavers). Second, if, for example, giant hollow trees and,
say, hole-nesting social woodpeckers or king-fishers coexisted long enough, our
argument would predict the evolution of eusociality. Third, if caves typically had
66 { General Foundations

structures in them such as hollow spheres with small openings (spheres that could
be expanded) then either birds or bats might have become eusocial.
Many small organisms live in apparently suitable sites yet have not evolved
eusociality. Some may have failed to do so because parental care is of little or no
value to them. Others, such as subsocial Embioptera, Gryllidae, Dermaptera,
Hemiptera, Coleoptera, Scorpionida, and Arachnida that live subsocially in seem-
ingly appropriate sites (but which, for one reason or another, may be too short-
lived), may lack the ability to initiate evolution of adequate defense of a nest site or
may not have been subsocial long enough. Many of these small forms are semelpa-
rous, and it seems obvious that the ancestors of all eusocial forms were iteropar-
ous. Semelparous adults are not likely to improve nesting sites significantly or to
create conditions leading their offspring to tarry at the nest. Moreover, even if
some offspring did tarry, there would be no younger siblings to help unless the
parents were iteroparous.
It may seem that eusociality should evolve much more easily in the tropics,
because it is easier to establish there the kind of more or less continuous breed-
ing that accompanies increasing colony size and continued nest defense. The life
cycle of temperate insects may usually be so set by the seasons as to make it quite
difficult to initiate continuous breeding as an aspect of the initiation of eusocial-
ity. This speculation seems to predict that persistent subsociality in the soil and
in wood may be more prevalent in temperate regions than in the tropics (when it
occurs in the tropics it is more likely to change to eusociality) and that eusocial
insects evolved in the tropics. However, the possibility of seasonality yielding the
selective situation that would lead to obligate workership in first broods without
altering life spans in workers or queens, as described above for Polistes fuscatus,
represents a counterargument.

Further Comments on Vertebrate Eusociality

It may be an oversimplification to assume that there are no eusocial vertebrates

except naked mole-rats (see also Lacey and Sherman, chap. 10). African hunting
dogs and wolves live in packs that hunt cooperatively. In some cases, one female
and one male have pups, and their offspring from the last season or two help them
rear the young, carrying back meat that they regurgitate for the pups and probably
protecting them and their parents from some kinds of danger (Lawick-Goodall
and Lawick-Goodall 1970; Mech 1970, 1988). Surely, helping in some of these spe-
cies regularly causes helpers to produce no offspring. But the social groups are
smaller than those of the eusocial insects, and there is no evidence yet of morpho-
logical divergence of parental and helper phenotypes.
Some cooperatively breeding birds behave like the social canines (Emlen 1984;
J. L. Brown 1987) and, possibly, beavers (Wilson 1975), dwarf mongooses (Rood
1978), and naked mole-rats (Jarvis 1981; Lacey and Sherman, chap. 10; Jarvis et al.,
 Eusociality in Naked Mole-Rats } 67

chap. 12; Faulkes et al., chap. 14). Some of these mammals and birds are similar to
some wasps and bees, in which groups are small; phenotypes have diverged little
or not at all among castes; obvious competition occurs among potential breeders;
and high proportions of helpers seem to be waiting and watching in case they get
the chance to breed.
In contrast to mammals, birds would appear to be significantly hampered
because they cannot simultaneously expand nest sites to accommodate large num-
bers of individuals and defend them in stationary locations on a multigenerational
basis. They do not possess sting equivalents to deal with the kinds of predators
that wasps and bees are able to deter, and, as a consequence, they are not able to
construct and use expansible nests equivalent to the exposed paper and mud nests
of Hymenoptera.
Helper and parental phenotypes may also have failed to diverge in vertebrates
because the jobs that parents and helpers do are very similar. Vertebrate workers
may not have the same opportunities as eusocial insects for magnificently repro-
ductive (family-saving) suicidal acts (probably in defense against vertebrates)
and the specializations improving the ability to do them (West-Eberhard 1975).
Canines probably lack the kinds of predators that could guide such evolution.
Birds may have the predators but nothing paralleling the venomous sting of female
Hymenoptera. One hymenopteran worker can deter either a huge predator (like
a human or a bear) that can destroy its whole family (of hundreds or thousands)
in one swipe, or a bumbler that could do it only by accident. By plugging a break
in the nest fortress, one termite can also deter a predator. It is more difficult for
most vertebrates to be such heroes, though such opportunities may exist for naked
mole-rats when predatory snakes enter their burrows (see Jarvis and Bennett
chap. 3; Brett, chap. 4; Braude, chap. 6).
Mammalian and avian social groups (other than “selfish herds “) never get
as big as those of the eusocial insects, and this also restricts the opportunities
for superreproductive heroism. The ultimate heroes among eusocial forms are
the polistine wasp and honey bee soldier-workers whose barbed stings cannot
be extracted, making their attacks on predators irreversibly suicidal. One pre-
dicts that barbed stings will be used for defense only in species that form new
colonies in swarms, such as honey bees and some tropical wasps. In very small
colonies, workers are too valuable for suicidal attacks to be beneficial. The only
other barbed stings are those of some ants, which evidently use them to kill prey
(A. Mintzer, pers. comm.), and those of the wasp genus Oxybelus, which uses
them to carry prey (Evans and West-Eberhard 1970); the prediction thus seems
to be met.
Another reason why the vertebrate reproductive and worker failed to diverge
sufficiently could be the relatively great behavioral plasticity of vertebrates, which
reduces the likelihood of the evolution of alternative phenotypes (separate and dis-
continuous; behavioral, physiological, and/or morphological). (Environmentally
determined alternative phenotypes have evolved thousands of times in insects,
68 { General Foundations

not merely in connection with social life, but much more frequently in regard to
dispersal in species in short-lived habitats, e.g., the phases of migratory locusts,
alary morphs in Orthoptera and Hemiptera, alternative phenotypes in successive
generations or on different hosts in aphids.) Assuming that vertebrate helpers
at the nest improve the reproduction of their parents or siblings, their failure to
evolve sterile castes may result from the absence of long-term predictable fluctua-
tions in the reproductive value of helping versus reproducing directly. Again, the
reversible flexibility of the individual vertebrate phenotype may be partly respon-
sible for damping the effective severity of such fluctuations, and the relatively
long lives and the iteroparity of vertebrates may have reduced the number of such
fluctuations.

Literature Cited

Braude, S.H. 1991. Which naked mole-rats volcano? In The Biology of the Naked Mole-Rat.
P.W. Sherman, J.U.M. Jarvis, R.D. Alexander, eds., pp. 185–194. Princeton, N.J.: Princeton
University Press.
Brett, R.A. 1991. The ecology of naked mole-rat colonies: Burrowing, food and limiting fac-
tors. In The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M. Jarvis, R.D. Alexander,
eds., pp. 137–184. Princeton, N.J.: Princeton University Press.
Brown, J.L. 1987. Helping and Communal Breeding in Birds. Princeton, N.J.: Princeton
University Press.
Emlen, S.T. 1981. Altruism, kinship, and reciprocity in the white-fronted bee-eater. In
Natural Selection and Social Behavior. R.D. Alexander and D.W. Tinkle, eds., pp. 217–
230. New York: Chiron Press.
Emlen, S.T. 1984. Cooperative breeding in birds and mammals. In Behavioral Ecology: an
Evolutionary Approach. 2d ed. J.R. Krebs and N.B. Davies, eds., pp. 305–339. Oxford:
Blackwell.
Evans, H.E. and M.J. West-Eberhard. 1970. The Wasps. Ann Arbor: University of Michigan
Press.
Faulkes, C.G., D.H. Abbott, C.E. Liddell, L.M. George and J.U.M. Jarvis. 1991. Hormonal
and behavioral aspects of reproductive suppression in female naked mole-rats. In
The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M. Jarvis, R.D. Alexander, eds.,
pp. 426–445. Princeton, N.J.: Princeton University Press.
Jarvis, J.U.M. 1981. Eusociality in a mammal: Cooperative breeding in naked mole-rat colo-
nies. Science (Wash., D.C.) 212:571–573.
Jarvis, J.U.M. and N.C. Bennett. 1991. Ecology and behavior of the family Bathyergidae. In
The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M. Jarvis, R.D. Alexander, eds.,
pp. 66–96. Princeton, N.J.: Princeton University Press.
Jarvis, J.U.M, M.J. O’Riain and E. McDaid. 1991. Growth and factors affecting body size
in naked mole-rats. In The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M. Jarvis,
R.D. Alexander, eds., pp. 358–383. Princeton, N.J.: Princeton University Press.
Koenig, W.D. and F.A. Pitelka. 1981. Ecological factors and kin selection in the evolution of
cooperative breeding in birds. In Natural Selection and Social Behavior. R.D. Alexander
and D.W. Tinkle, eds., pp. 261–280. New York: Chiron Press.
 Eusociality in Naked Mole-Rats } 69

Lacey, E.A. and Sherman, P.W. 1991. Social organization of naked mole-rat colonies: evi-
dence for division of labor. In The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M.
Jarvis, R.D. Alexander, eds., pp. 274–357. Princeton, N.J.: Princeton University Press.
Lawick, H. van, and J. van Lawick-Goodall. 1970. Innocent Killers. London: Collins.
Mech, L.D. 1970. The Wolf: The Ecology and Behavior of an Endangered Species. New York:
Natural History Press.
Mech, L.D. 1988. The Arctic Wolf: Living with the Pack. Stillwater, Minn.: Voyageur Press.
West-Eberhard, M.J. 1975. The evolution of social behavior by kin selection. Q. Rev. Biol.
50:1–33.
Wilson, E.O. 1971. The Insect Societies. Cambridge, Mass.: Belknap Press of Harvard
University Press.
Wilson, E.O. 1975. Sociobiology: The New Synthesis. Cambridge, Mass.: Belknap Press of
Harvard University Press.
4}

Parent-Offspring Conflict and Manipulation

Life Effort
dogs
crossing streets
as if they had some place to go
people
hurrying
as if time were short
people
crossing streets,
as if they had some place to go
dogs
hurrying
as if time were short
Alexander, 2011, p. 18
 INTRODUCTION: THE EVOLUTION OF SOCIAL BEHAVIOR
David C. Queller

Richard Alexander’s 1974 paper, “The evolution of social behavior” (Alexander

1974) probably marks the watershed publication in his career. Most of his pre-
vious papers are about acoustical communication or systematics, particularly in
orthopterans. Most of his later ones are on questions of social evolution. Perhaps
Alexander’s orthopterans were like Darwin’s barnacles, the empirical foundation
for bigger ideas. This is not to trivialize the earlier work; it earned him election to
the National Academy of Sciences. It must be very unusual for an Academy mem-
ber to do his or her best work after they are elected, because of age, complacency,
or just regression on the mean. But Alexander did.
The 1974 paper is an early attempt to describe a general theory of social behav-
ior. It follows on Williams (1966) critique of loose group selection thinking, and
on the work of Hamilton (1964a, b, 1966, 1967, 1972) and Trivers (1971, 1972) in
building an individual-centered theory. Alexander was well ahead of the curve
here; a wider recognition of these issues would begin to come only later, with the
publication of Sociobiology (Wilson 1975) and The Selfish Gene (Dawkins 1976).
Alexander argued that the fabric of social evolution is woven from three classes
of behavior: nepotism, reciprocity, and parental manipulation. He applies these
concepts to why groups form (primarily for protection against predators) and to
why social behavior evolves within groups (primarily from increased reproduc-
tive competition). He then moves to several particular topics including parental
manipulation in humans and the evolution of social insects, the latter of which is
the portion reprinted here.
So there is a special pleasure in introducing this paper that broke ground in our
understanding of many topics in social evolution. Less pleasurable is the need to
mention a rather large error in the paper, but I know Alexander won’t mind. In the
early 1980s I remember him cheerfully telling everyone that the reason this paper
had been so heavily cited was that it included this mistake. That’s not an accurate
assessment of the paper, but it gives on an accurate view of Alexander’s spirit of
inquiry and intellectual honesty. If you don’t make an occasional mistake, you are
probably not thinking as creatively as you ought to be.
The error concerns the last of Alexander’s trio of social mechanisms, parental
manipulation. From inclusive fitness theory, and from a not-yet-published article
of Trivers (Trivers 1974), he knew that parents and offspring could have conflict-
ing interests about parental care. An offspring that gets more parental resources
72 { General Foundations

decreases resources available to other offspring. Parents and offspring view this
trade-off differently because of different relatednesses. A parent is equally related
to all offspring but each offspring is most related to itself.
Alexander thought that parents would win in conflicts with their offspring, for
two reasons. The first was that parents were more powerful, not just in the sense
of being larger, but also because parents are the dispensers of resources and can
withhold those resources if that is in their interests. I will return to this important
theme shortly.
The second reason is the erroneous one. Alexander reasoned that offspring
could not evolve to act selfishly against the interests of their parents because, when
they later become parents, the roles are reversed; they will pass this selfish gene on
to their offspring and suffer as a result. Qualitatively this role-reversal argument
is quite correct, but it takes mathematics to show whether it holds quantitatively.
Does the selfish offspring lose just as much when it becomes a parent as it gained
earlier in life? It turns out that relatedness captures the quantitative aspect. Yes,
a selfish offspring passes on its selfish genes to its offspring, but they are diluted
by the half of the offspring’s genes that come from elsewhere, and it is this half
that makes the difference. The first mathematical model directly addressing this
point was by a graduate student at Michigan, James Blick (Blick 1977), stimulated
and encouraged by Alexander, who promptly changed his mind about the ques-
tion. Subsequent models quickly confirmed this finding (Macnair and Parker 1978;
Parker and Macnair 1978; Stamps et al. 1978). In some sense that had to be true if
inclusive fitness theory was correct. If offspring have the same interests as their
parents, and their parents have the same interests as the grandparents, and so on,
then individuals would be following the collective interests of innumerable over-
lapping remote ancestors.
The error was not too serious for the rest of the paper for a number of reasons.
First, despite his role-reversal argument that implies that offspring must follow
parental interests, Alexander sometimes argues in a way that implies that their off-
spring’s inclusive fitness does matter. For example, he notes that, except in clonal
groups, the interests of individuals in a group are never identical. Similarly he
argues that the amount of genetic overlap (relatedness) determines the amount
of parental molding necessary to get offspring to cooperate. This seems difficult
to reconcile with his argument that parents must win. But is more like how we
would put the argument today based on parental manipulation of offspring inclu-
sive fitness options. Parents can do things to offspring that change the offspring’s
inclusive fitness payoffs and therefore offspring behavior.
Second, even though the role-reversal argument was not correct, parental
manipulation is real and important for the other reasons Alexander gave, chiefly
the relative power of the parent. It seems significant that morphological castes in
social insects are normally determined by nutrition, over which parents would
likely have strong control. A mother might benefit from feeding some of her off-
spring less food if that makes them less able to reproduce but still able to be effective
 Parent-Offspring Conflict and Manipulation } 73

helpers (West-Eberhard 1978; Craig 1979). However, this idea was not supported
in two experimental tests in primitively eusocial wasps (Queller and Strassmann
1989; Field and Foster 1999) so it is still an open question how important this was
for the origin of eusociality. Still, at some point in the elaboration of eusociality
nutrition becomes important so that there are opportunities for parents, and for
older workers, to manipulate the caste of younger workers. The importance of this
control is shown by the consequences of its absence in the stingless bees in the
genus Melipona (Ratnieks 2001; Wenseleers and Ratnieks 2004). Here all female
offspring are fed equally, and a large fraction of them selfishly opt to develop as
queens even though few queens can be supported in this swarm-founding group.
Most are therefore killed by the workers.
Finally, Alexander was able to focus on important empirical points that were
valid even if they were motivated in part by a mistaken theory. In arguing that
kin selection on offspring was not the primary force in eusociality, Alexander
questioned the evidence for Hamilton’s (1964b, 1972) haplodiploid hypothesis.
This idea, that eusociality with female workers is particularly easy to evolve in
haplodiploids because females were more related to their sisters (3/4) than to
their offspring (1/2), seemed to be the great success of kin selection theory. It
appeared to explain why so many origins of eusociality occurred in the haplodip-
loid Hymenoptera, why their workers were always female (while diploid termites
had workers of both sexes), and why workers never lay female eggs but some-
times laid male eggs.
Alexander questioned all three of these points, pointing out that there were
strong alternative explanations. The Hymenoptera are the most parental of insects,
so it is not surprising that they would easily evolve allo-parental care; all it requires
is a shift in who received the care. In addition, parental care in the Hymenoptera
is almost entirely done by mothers, not fathers, so it is not surprising that females
would most easily evolve allo-parental care. Finally, the restriction of worker
reproduction to sons might have the simple proximate explanation that sons are
all they can produce unless they undergo the risks of mating, and that the ability is
useful if the queen dies. These are solid arguments that stand today.
On some important points, there was a lack of sufficient data. Alexander
pointed out that the haplodiploid hypothesis depends on single mating by the
queen, while Alexander’s parental manipulation hypothesis did not. While noting
the paucity of information on this important point, he was misled by the example
of the highly promiscuous honeybee into thinking that multiple mating might be
common. In the years since, with the aid of molecular methods, mate number has
been determined for many species of social insects. A recent phylogenetic analysis
of mate number data for 267 eusocial species (Hughes et al. 2008) showed that,
although multiple mating occurs, it is always derived. Every origin of eusociality
appears to have occurred in a singly mated species and multiple mating may have
evolved only after workers were locked into their roles.
74 { General Foundations

On another point with little data, Alexander was correct. He noted the absence
of evidence for nepotism within colonies. For example, why do workers not favor
full sisters over half sisters? This generalization has become stronger over the years
(Keller 1997), and remains something of a puzzle.
But other data would eventually show that relatedness certainly does matter,
and that offspring can sometimes win in conflicts with parents. The key results
came from sex ratios (Trivers and Hare 1976). In haplodiploids with singly mated
queens, female workers are three times more related to sisters than to brothers and
are therefore selected to favor three times as much investment in sisters. Queens,
in contrast, favor the standard 1:1 investment ratio in sons and daughters. Trivers
and Hare (1976) supported the prediction of worker control using comparative
analyses. These were initially questionable (Alexander and Sherman 1977), but
support for the predictions has become very strong over the years (Nonacs 1986;
Queller and Strassmann 1998; Chapuisat and Keller 1999). Today, key questions for
sex ratio conflicts and other queen-worker conflicts concern who controls what
levers of power (Beekman and Ratnieks 2003), and how conflicts get resolved
(Ratnieks et al. 2006).
Much of the importance of Alexander’s analysis comes from a shift in empha-
sis from relatedness to ecological benefits. Although we know that relatedness is
essential, differences in relatedness had been overemphasized compared to the
equally essential differences in ecological costs and benefits that form the rest of
Hamilton’s rule. Arguing from the example of termites, where haplodiploidy plays
no role, Alexander suggested that the key to eusociality was a nest that constituted
a valuable resource that could be utilized over multiple generations. This insight
could be true under either parental manipulation or kin selection and Alexander
later developed this idea further under a kin selection framework (Alexander et al.
1991). He argued that eusociality was particularly favored when nest sites were safe
or defensible, long-lasting, initially small, and expansible, and food rich.
In general, there is a great deal of continuity between the thinking in the 1974
and 1991 papers, despite the shift from a parental manipulation emphasis to a kin
selection emphasis (though with parental manipulation still involved). To under-
stand eusociality we need not just relatedness, but ecological benefits and costs.
We need to understand why alloparental care evolves not just in the Hymenoptera
but in termites and vertebrates. In addition, we need to understand not just the
workers, but also the reproductives.
I have focused on eusociality in order to match the section of the paper
reprinted, but the contributions of the paper are much broader, including not
only the major themes mentioned earlier, but also some very significant points
mentioned only briefly. His comments on disease being a nearly unavoidable con-
sequence of grouping predated the now generally acknowledged importance of
pathogens in ecology and evolution (Schmid-Hempel 2011). Alexander’s argument
on page 350 explains how a dominant individual might concede some reproduc-
tion to a subordinate in order to keep it in the group, a foreshadowing of skew
 Parent-Offspring Conflict and Manipulation } 75

theory (Keller and Reeve 1994). On page 353, Alexander discusses how helping a
relative may not be as easy to evolve as Hamilton’s equations implied if the rela-
tives are also particularly close competitors, again anticipating a lot of later theory
(Taylor 1992; Wilson et al. 1992; Queller 1994; Van Dyken 2010). Most important,
significant parts of the paper are devoted to human behavior and presage much of
Alexander’s pioneering work on this topic.

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Alexander, R.D. 2011. The Mockingbird’s River Song: Poems, Essays, Songs and Stories, 1946-
2011. Manchester, MI: Woodlane Farm Books.
Alexander, R.D. and Sherman, P.W. 1977. Local mate competition and parental investment:
patterns in the social insects. Science 196:494–500.
Alexander, R.D., Noonan, K.M., and Crespi, B.J. 1991. The evolution of eusociality. In: P.W.
Sherman, J.U.M. Jarvis, and R.D. Alexander (eds.), The Biology of the Naked Mole-Rat.
Princeton, NJ: Princeton University Press, pp. 3–44.
Beekman, M., and Ratnieks, F.L.W. 2003. Power over reproduction in social Hymenoptera.
Phil. Trans. R. Soc. Lond. B. 358:1741–1753.
Blick, J. 1977. Selection for traits which lower individual reproduction. J. Theoret. Biol.
67:597–601.
Chapuisat, M., and Keller, L. 1999. Testing kin selection theory with sex allocation data in
eusocial Hymenoptera. Heredity 82:473–478.
Craig, R. 1979. Parental manipulation, kin selection, and the evolution of altruism. Evolution
33:319–334.
Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press.
Field, J., and Foster, W. 1999. Helping behavior in facultatively eusocial hover wasps: an
experimental test of the subfertility hypothesis. Anim. Behav. 57:633–636.
Hamilton, W.D. 1964a. The genetical evolution of social behaviour. I. J. Theoret. Biol. 7:1–16.
Hamilton, W.D. 1964b. The genetical evolution of social behaviour. II. J. Theoret. Biol.
7:17–52.
Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theoret. Biol.
12:12–45.
Hamilton, W.D. 1967. Extraordinary sex ratios. Science 156:477–488.
Hamilton, W.D. 1972. Altruism and related phenomena, mainly in the social insects. Annu.
Rev. Ecol. Syst. 3:193–232.
Hughes, W., Oldroyd, B., Beekman, M., and Ratnieks, F. 2008. Ancestral monogamy shows
kin selection is key to the evolution of eusociality. Science 320:1213–1216.
Keller, L. 1997. Indiscriminate altruism: unduly nice parents and siblings. Trends Ecol. Evol.
12:99–103.
Keller, L., and Reeve, H.K. 1994. Partitioning of reproduction in animal societies. Trends
Ecol. Evol. 9:98–102.
Macnair, M.R., and Parker, G.A. 1978. Models of parent-offspring conflict, II. Promiscuity.
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Parker, G.A., and Macnair, M.R. 1978. Models of parent-offspring conflict. I. Anim. Behav.
26:97–110.
Queller, D. 1994. Genetic relatedness in viscous populations. Evol. Ecol. 8:70–73.
Queller,D.C., and Strassmann,J.E. 1989. Measuring inclusive fitness in social wasps. In:
Breed, and R. E. Page (eds.), The Genetics of Social Evolution. Boulder, CO: Westview
Press, pp. 103–122.
Queller, D.C., and Strassmann, J.E. 1998. Kin selection and social insects. Bioscience
48:165–175.
Ratnieks, F., Foster, K.R., and Wenseleers, T. 2006. Conflict resolution in insect societies.
Annu. Rev. Entomol. 51:581–608.
Ratnieks, F.L.W. 2001. Heirs and spares: caste conflict and excess queen production in meli-
pona bees. Behav. Ecol. Sociobiol. 50:467–473.
Schmid-Hempel, P. 2011. Evolutionary Parasitology: The Integrated Study of Infections,
Immunology, Ecology, and Genetics. Oxford: Oxford University Press.
Stamps, J., Metcalf, R., and Krishnan, V. 1978. A genetic analysis of parent-offsping conflict.
Behav. Ecol. Sociobiol. 4:369–392.
Taylor, P.D. 1992. Altruism is viscous populations—an inclusive fitness model. Evol. Ecol.
6:352–356.
Trivers, R.L. 1971. The evolution of reciprocal altruism. Q. Rev. Biol. 46:35–47.
Trivers, R.L. 1972. Parental investment and sexual selection. In: B. Campbell (ed.), Sexual
Selection and the Descent of Man. Chicago: Aldine.
Trivers, R.L. 1974. Parent-offspring conflict. Am. Zool. 14:249–264.
Van Dyken, J.D. 2010. The components of kin competition. Evolution 64:2840–2854.
Wenseleers, T., and F.L.W. Ratnieks. 2004. Tragedy of the commons in Melipona bees. Biol.
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West-Eberhard, M.J. 1978. Polygyny and the evolution of social behavior in wasps. J. Kansas
Ent. Soc. 51:832–856.
Williams, G.C. 1966. Adaptation and Natural Selection: A Critique of Some Current
Evolutionary Thought. Princeton, NJ: Princeton University Press.
Wilson, D.S., Pollock, G.B., and Dugatkin, L.A. 1992. Can altruism evolve in purely viscous
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Wilson, E.O. 1975. Sociobiology: The New Synthesis. Cambridge: Harvard University Press.
 THE EVOLUTION OF SOCIAL BEHAVIOR

Excerpt from Alexander, R.D. 1974. The Evolution of Social Behavior, Annual
Review of Ecology and Systematics 5:357-367.

Evolution of Sociality In Insects

The social insects have been a central theme in every major publication on natural
selection for one important reason: they are apparently alone among all organisms
in having evolved obligately sterile individuals. Darwin (41. p. 236) referred to the
sterile castes of insects as the “one special difficulty, which at first appeared to me
insuperable, and actually fatal to my whole theory.” Darwin effectively solved the
problem of how different kinds of sterile castes can evolve within a single spe-
cies by realizing that selection can operate through the “family.” As he put it (41,
p. 238) ‘‘a breed of cattle, always yielding oxen with extraordinarily long horns,
could be slowly formed by carefully watching which individual bulls and cows,
when matched, produced oxen with the longest horns; and yet no one ox could
ever have propagated its kind.”
Nevertheless, as Hamilton (67) indicates, the problem of precisely how obli-
gate sterility has evolved in the various social insects is still with us. As the most
extreme form of altruism known, its relationship to everything said about social
behavior up to this moment is obvious. Indeed, the social insects are probably
the best example available for distinguishing the predictions and correlates of the
three general systems of selection in social groups.
Several lengthy and detailed discussions of the probable selective backgrounds
of insect sociality have been published recently (11, 50, 60, 67, 101, 109, 110, 166,
168, 169, 171, 173- 175). The following account is by comparison a brief and sketchy
effort in which I shall attempt to distinguish in certain specific regards the predic-
tions and correlates of theories principally invoking 1. reciprocity, 2. kin selection,
and 3. parental manipulation of progeny.
Since Hamilton’s (60) paper, with the principal exception of Michener (110)
and Lin & Michener (101), only kin selection, in which each individual worker
or soldier caste is expected to secure an overcompensating genetic return for its
altruism, has been invoked to explain altruism in eusocial insects. Across the past
several years: however, I have become convinced that kin selection is not a suf-
ficient explanation for such behavior in insects, and that it may be only feebly and
infrequently involved. Kin selection, I suggest, will prove ultimately to be most
78 { General Foundations

relevant to the kinship and breeding systems of primate and human societies, for
only there does clear evidence exist of keen ability to discriminate among many
different relatives within social groups. [Curiously. Hamilton (67) makes the same
suggestion for reciprocity.] The broad applicability of Hamilton’ s (60, 67) papers,
and the changes in approach that they have caused, place them among the most
important theoretical contributions to evolutionary biology since Fisher. But
I believe that in some respects Darwin was more nearly correct than Hamilton,
and that a form of parental manipulation of progeny in the interests of the par-
ent best explains the sterile castes of insects. The difference between these two
arguments can be clarified by referring to Hamilton’s (60) summary statement
(p. 29) “If a [hymenopteran] female is fertilized by only one male all the sperm she
receives is genetically identical. Thus, although the relationship of a mother to her
daughters has the normal value of 1/2, the relationship between daughters is 3/4.
..other things being equal, [a newly adult daughter would prefer] returning to her
mother’s [nest] and provisioning a cell for the rearing of an extra sister to provi-
sioning a cell for a daughter of her own. From this point of view therefore it seems
not surprising that social life appears to have had several independent origins in
this group of insects.”
If, however, other things are indeed equal, then queen offspring of the above
monogamous female cannot maximize their inclusive fitnesses by their devotion
to producing offspring only half like themselves. Only if we assume that the parent
has evolved to mold or manipulate her offspring phenotypically so as to maxi-
mize her own reproduction can both worker and queen offspring maximize their
respective inclusive fitnesses. This they can do because of the particular pheno-
types with which the mother endows each of them as a result of the distribution of
parental benefits and influences. Such an idea does not detract from the underly-
ing significance of kin selection in sexual organisms. The amount of genetic over-
lap of different individuals must still determine the amount of parental molding
necessary to effect cooperation. Nevertheless, it is clear that individual offspring
consistently appearing in the same situations are unlikely on the basis of kin selec-
tion alone to evolve dramatically different roles in which one is a sterile helper
at the nest and one reproduces in the normal fashion. Furthermore, so long as it
is parental manipulation that brings about sibling cooperation, genetic relation-
ships among siblings indicate only the amount of parental molding necessary, not
whether or not it will be able to yield a given result. Alternative explanations for
the prevalence of eusociality among Hymenoptera, and for its presence in male-
diploid termites, are thus given more credibility.
The eusocial insects actually have two distinctive attributes: sterile castes and
overlap of the mother’s reproductive life with that of her offspring. Social groups
with these attributes appear to derive from two different precursors: l. groupings of
subsocial (parental) females (eventually including their offspring) and 2. extended
families of single mothers. In either case extended parental care precedes eusocial-
ity and sterile castes. This apparent dichotomy has long puzzled students of insect
 Parent-Offspring Conflict and Manipulation } 79

social behavior, and is in fact responsible for much of the disagreement in recent
theoretical arguments (101, 109, 110). The similarity of the two groups is greatest if
the groups of subsocial females, in cases that lead to eusociality, are always sibling
groups. Then, as Lin & Michener (101) note, the only difference would be that in
one case the mother is present and in the other she is not. As a result, the problems
of selection during evolution of sterile castes become essentially the same in the
two cases. Because (a) single-queen colonies are vastly preponderant in eusocial
insects, (b) facultative sterility has not been unequivocally demonstrated among
nonsiblings, and (c) for reasons already indicated it is much easier to evolve sterile
castes among siblings, I here suggest that the burden of proof may be upon the
investigator who argues that sterile castes have evolved other than within broods
of single mothers.
In this light we can begin our comparison by considering Michener’s (109) pro-
posal that groups of cooperating unrelated female bees evolved through stages in
which differences in reproduction among them came to be actual division of labor
in reproduction, and then led directly to the evolution of sterility in some of the
females. Lin & Michener (101) defended this idea, but with the critical modifica-
tion that the cooperating females may (sometimes!) be siblings.
As was shown above, in systems of reciprocity, each individual is continually
gambling that his investment will improve both his phenotypic and his genotypic
fitness; indeed, what is going on is a form of mutual exploitation under the ben-
efits of group living. There is in fact no altruism except in a temporary sense that
benefits may be given at one time and received only at a later time. Should systems
of pure reciprocity exist, evolution will tend to reduce fitness shifts to zero—that
is, to equalize investments and benefits to individuals. There is no alternative, and
this is the precise opposite of what has to happen in the evolution of obligate steril-
ity. As a result we can dismiss reciprocity as being the central factor in the evolu-
tion of sterile castes.
Bees or other parental insects may have interacted reciprocally in groups prior
to the evolution of sterile castes, and they may have done so subsequent to the
evolution of sterile castes. Different families of social insects in a single large group
of the sort that are sometimes called “multiple-queen colonies” may even use ster-
ile individuals now as their social donations, or their contributions to reciproc-
ity in the maintenance of the entire group of families, as can also be proposed
for facultatively sterile individuals in human religious sects. Group living among
competing reproductives may have evolved among subsocial bees for any of the
reasons for group living given earlier, and such group living may have [as Lin &
Michener (101) suggest] somehow “primed” siblings in the direction of forming
groups within which sterile castes could evolve. When such groups are composed
of closely related nonsiblings, eusociality could feasibly evolve through kin selec-
tion; but this route seems less likely than the route of parental manipulation, for
reasons out lined below. In no other sense can the interactions of unrelated com-
peting reproductive females lead to evolved sterility.
80 { General Foundations

In distinguishing the predictions and the correlates of kin selection and parental
manipulation in accounting for sterile insect castes let us first consider the genetic
relationship of altruist and beneficiary. A principal difference between kin selec-
tion and parental manipulation is that kin selection, as formulated by Hamilton
(60), requires that each individual secure genetic returns for its altruism greater
than the cost of the altruism to its own personal reproduction, this return deriving
from the likelihood that given relatives will carry a gene for altruism carried by the
altruist. To the extent that the evolution of parental care has placed parents in the
position of being able to use their investments in some offspring to increase their
total reproduction via other offspring, this requirement is nullified.
Genes for altruism among siblings that benefit the parent can spread regardless
of their distribution in the brood with respect to dispensation of altruism. I believe
that this fact may largely solve the problem of initially saving and spreading genes
causing their bearers to be altruistic, advantages to parents thus perhaps providing
a major source of genes leading to altruism in all contexts (including the tempo-
rary altruism of reciprocity). The significance of this explanation in accounting
for phenomena such as aposematic coloration is obvious (see also 53). Thus the
parent with a few brightly colored offspring in a poisonous brood may be both
more likely to lose the brightly colored offspring and more likely to produce a big-
ger brood after predation. The allele for brighter color, assumed for this example
to be recessive and present in other individuals in broods having a few homo-
zygous bright individuals, may as a result be selected downward within broods
while simultaneously being selected either downward or upward in the species or
population as a whole. (See also Figure 1, Brood 1-2c-3c.)
While this situation continues (meaning until the alleles for aposematic color-
ation have spread widely), the selection that is going on will favor the parent who
produces at least a few homozygous bright offspring, disfavor homozygous bright
offspring, and either favor or disfavor alleles for brightness, depending upon the
intensity and kind of selection. lt may also favor parents whose offspring tend to
cluster around the few bright offspring, probably to the added detriment of those
individuals since they will likely be more obvious to predators in the middle of a
group of moving caterpillars than when alone. If a mutant for brightness is not
entirely recessive then its initial spread may be inhibited more than in the above
example, except that a heterozygous parent will produce an entire partly bright
brood. This example purposely omits the possibility of predators with a general-
ized ability (of whatever origin) to avoid brightly colored potential prey. In such
cases alleles for brightness will be favored in all circumstances.
Let us now consider the genetic relationships of altruists and beneficiaries
among social insects. Hamilton and others have emphasized the 3/4 average genetic
relationship of sisters in a hymenopteran social colony, given the haplo-diploid
sex-determining mechanisms of all Hymenoptera and a monogamous mother.
This emphasis is misleading for three reasons. First, the termites, which have also
evolved eusociality, have normal diploid males. Second, as pointed out by Trivers
 Parent-Offspring Conflict and Manipulation } 81

(158), only the females are considered but brothers are also reared by workers, and
in haplo-diploid species they are only 1/4 like [and 1/4 unlike!] their sisters. Third,
eusocial hymenopteran queens at least frequently mate with more than one male.
Considering its importance, relatively little attention has been paid to the mating
of social Hymenoptera. Astonishingly, it was only recently discovered (Parker, ref.
124, lists references) that multiple inseminations (as many as 7-12 per queen) are
evidently the rule in honeybees (each male can mate only once). Single mating has
been established for few social hymenopteran females, but multiple insemination
is apparently common (101. p. 141; 124; 175, p. 330).
There is no evident correlation between monogamy and eusociality or tenden-
cies toward eusociality. It is possible, but not convincing in view of the generally
polygynous or promiscuous hymenopteran background, to postulate 1. brief peri-
ods of monogamy in each line that became eusocial and 2. that once sterile castes
had evolved, multiple matings could become the rule even if monogamy were
critical in the appearance of sterility. Wilson (175, p. 33), after noting that multiple
insemination “is not favorable to Hamilton’s thesis” suggests l. the above explana-
tions and 2. the possibility that males are often closely related. But the necessarily
dangerous mating flights of queen honeybees (compared to mating on the comb),
even though drones have access to hive interiors, suggests selection favoring out-
breeding; the appearance under inbreeding of useless diploid males that are killed
in the pupal stage by the workers (83, 135, 178) suggests a long history of outbreed-
ing. Hymenopteran siblings may average a closer relationship than siblings in spe-
cies with diploid sexually produced males, but a 3/4 average relationship is yet to
be demonstrated. A point which detracts from the hypothesis suggested here is
the tendency of the sperm of different honeybee males to clump inside the queen
(152). This phenomenon reduces the variation in genetic relationships among the
hive members at most times. But this phenomenon may be widespread (124), and
there seems to be no evidence that it has been elaborated in honeybees because of
a value in regard to kin selection (also, see below).
Monogamy in termites probably long preceded eusociality coinciding with
extended parental care and ensconcement in burrows or crevices. Such behavior
is widespread among orthopteroid insects; Alexander (2) has provided a hypo-
thetical scheme indicating some of the steps by which this behavior could lead to
eusociality. The nesting cavity of termites (as well as the nests of wasps and bees)
is a resource possibly of value to breeding offspring. Parents could gain if adult
offspring sometimes remained in the cavity because of the opportunity of taking
it over from the parents when they died. Parents could gain further by 1. keeping
such offspring from engaging in deleterious competition over the nest resource
and 2. causing them to use their parental behavior in the parent’s interest when
healthy parents and adult offspring overlap. Long-lasting nests and overlap of par-
ents and offspring serving as facultative workers would in turn select for longer
parental life, and ultimately perhaps, for obligately sterile offspring. Abilities of
parents to make their offspring helpers would often tend to increase the duration
82 { General Foundations

of the nest as a reproductive resource and reinforce the entire process. I believe
that this hypothetical scheme may be generally applicable in accounting for insect
eusociality, and for at least some cases of extended families in vertebrates.
The central role of the duration of the nest resource in the above hypothesis
focuses interest on the manner in which nests are founded or pass from one gener-
ation to another. In this connection, West-Eberhard (168, pp. 66-67) has described
a series of intense conflicts across several weeks among potential queens of the
tropical paper wasp, Polistes canadensis, for possession of a 22-cell nest that had
five foundresses when first observed. These queens may or may not have been
sisters. Likewise, West-Eberhard describes as “offspring” three queens that fought
for the nest for three weeks after the dominant queen was removed; she does not
term them sisters, although they likely were. The evolutionary background of
this kind of conflict can only be understood through knowledge of the frequency
with which P. canadensis nests are usurped by nonsibling queens. West-Eberhard
describes several usurpations, but with little knowledge of the relationships of the
contending queens.
A parallel to the parent-offspring interactions in the above evolutionary situ-
ation can be drawn with long-lived trees. So long as the insect nest, as a repro-
ductive resource, persists longer than the incipiently social queen, there will be
selection for longer adult life; with trees, a similar effect accrues from persistence
of the resource of a place in the sun and soil. Both the tree and the insect are then
in competition with offspring for the resource, but the evolution of offspring that
compete with a healthy parent will be thwarted in either case. One predicts, as a
result, that seedlings will be less able to grow up under their own parents (e.g.,
165) than will seedlings of other species, which can evolve to compete; and within-
species allelopathy should be viewed as a parent-offspring interaction, rather than
simply intraspecific competition leading (for example) to some kind of population
regulation.
A healthy tree with a long life ahead of it gains only from offspring that ger-
minate somewhere other than beneath it, and it loses from those that germinate
beneath it. The extent to which parental poisoning of young will evolve, if it is not
genotype specific within species, will be determined by the frequency with which
seedlings germinating beneath conspecific adult trees do so beneath their own
parents; if the adult is often enough a nonparent, competitive ability will evolve in
the seedlings too. Trees should also evolve so as to maximize their likelihood of
replacement by an offspring, however, and with certain combinations of lengths
and predictabilities of juvenile and adult life, the result will be greater likelihood,
at least at certain times, of seedlings succeeding under their own parents. The pro-
duction of suckers or sprouts from roots of dying or afflicted trees must reflect a
history of success in trees replacing themselves, in this case by genetically identical
offspring.
With trees there is no obvious capability of evolving to use some juvenile seed-
lings to produce and rear others, so the competition can be clarified (partly) in
 Parent-Offspring Conflict and Manipulation } 83

terms of Hamiltonian kin selection: The tree is more interested in producing fur-
ther offspring of its own (1/2 like it) than in giving up the resource to its offspring
so that they can produce grandchildren (1/4 like it), particularly if the replacement
is likely to be a single offspring. The same is true of the insect (and it is particularly
important that in each case the resource is suitable for a single reproductive indi-
vidual). But this description does not specify why the parent wins in the competi-
tion, nor does it explain the evident “altruism” of the offspring. The social insect
differs from the tree in that, being already parental and with parentally inclined
offspring ready to assume ownership of the next resource, it is evidently only small
steps away from the capability of using those offspring as effective parental invest-
ment contributing to the reproduction of other offspring. Once assistance of par-
ents is seen in this light, the step to obligate sterility in some offspring is easy to
envision. It is possible that, in explaining insect eusociality, more attention should
be given to the effects of evolving the potential for producing a reliable and per-
sistent (homeostatic) environment useful to a single adult, which in turn selects
for longer adult life (as in trees), causing particular kinds of parent-offspring
competition.
The hypothesis that sterile insect castes evolved in the context of assisting the
reproduction of their parents thus leads to predictions somewhat different from
those of Hamiltonian kin selection. Sterile offspring may in this hypothesis be
totally altruistic, for no genetic return is required except to the parent (or, to say
it another way, to the brood as a whole). The sterile offspring are only a part of
the mother’s parental investment, and genetic relationships among the brood,
sex determining mechanisms, and numbers of matings by the mother may all be
more or less irrelevant. The reason is that the correlation is not with altruism being
directed at close relatives, but with altruism being directed at siblings, whose rela-
tionships to the mother (for each sex) are always the same.
Supporting the hypothesis that eusociality in the Hymenoptera derives from
the prevalence or extensive parental care, which has no great relevance in itself
to male haploidy, is the fact that parasitic Hymenoptera and the plant feeders of
the suborder Symphyta possess the male-haploid system of sex determination,
no extensive parental care, and no social behavior. Likewise the termites evolved
eusociality without male haploidy.
It appears that the critical factor in the evolution of eusociality is overlap of
breeding parents with adult offspring or extensive parental care of siblings in an
environment favoring cooperative nest-founding (therefore genes in the parent
causing sibling offspring to cooperate in the parent’s interests whether or not the
parent is present). One of the difficulties experienced by entomologists in apply-
ing their usual precise definitions has involved the question of whether or not
“true” social life (eusociality) should require only that parents tend their offspring
to adulthood or that there be in addition sterile castes. The reason the problem
has existed is that no parental insects are known to tend their offspring to adult-
hood, and overlap with them, without having sterile castes. The closest, perhaps,
84 { General Foundations

is Halictus quadricinctus, in which the mother remains in the nest “and is still
present when the first of her offspring emerge” (175; see 101, pp. 146-47, for other
doubtful cases). This virtual absence of parents in the same nest overlapping adult
offspring without sterile workers further argues that it is parent-offspring interac-
tions and not selection on sibling interactions as such that is involved in eusocial-
ity. Eusocial insects are unusual in having parents that overlap the total adult life
of some offspring. Even of successions of offspring.
Regarding the relationships of sister workers in the Hymenoptera it is also rele-
vant that with, say, two matings by the mothers the sisters may average 50% genetic
overlap (or more: see 67), but with two haploid fathers their relationships actually
vary more than they would with a single diploid father because the haploid sperm
contributions of two different fathers cannot recombine. Some pairs of workers
will overlap genetically much more than others; this point has never been made
clear, and one result is that efforts to apply kin selection, (e.g., 27. 28, 50) have con-
sidered only average relationships and thus between-group selection. The lack of
evidence of within-colony discrimination in single-queen species, even given two
or more fathers, calls forth the spectacle of nurse bees sometimes tending young
queens with whom they share relatively few genes. Again, it is to the mother’s
advantage (although not to the fathers’, in the case of multiple mating) that sis-
ters treat each other alike. Although Hamilton (60, 67) believes that worker laying
indicates worker reluctance to raise the queen’s male offspring, discrimination by
workers against the queen’s male offspring has apparently not been reported, and
other explanations for worker laying are likely (see below). If bees and other social
insects can discriminate offspring of different mothers within multiple-queen col-
onies (evidence of aggression among workers in multiple-queen colonies would
represent the critical datum), and if kin selection is the main force in the evolu-
tion and maintenance of worker altruism, it is legitimate to wonder why workers
with different fathers have not evolved the ability to discriminate full and half
siblings. If altruism is a matter of queens manipulating their parental investments,
this problem ceases to exist.
A second problem involves the question of why there are no male workers in
the Hymenoptera. The kin selection argument is that, because of their haploidy,
they are less closely related to one another and to their sisters, hence have less
stake in the colony (60). But there is another much more compelling explanation.
First, males are rarely parental in the Hymenoptera, social or not (see 175 for the
possibility of specialized exceptions among ants), although the females are more
parental than perhaps any other insects. More importantly, the hymenopteran
female controls the sex ratio of her brood by fertilizing or not fertilizing her eggs.
As a parent she can therefore produce whatever proportion of females (thus, what
ever proportion of workers) is most advantageous to her in the immediate situ-
ation. Under these conditions it is scarcely necessary to invoke kin selection to
explain the absence of the genetic revolution necessary to make hymenopteran
males parents. As Trivers & Willard (159) point out, the altruism from female
 Parent-Offspring Conflict and Manipulation } 85

progeny toward male progeny, in this case without compensating genetic return,
will favor parents able to produce appropriately greater proportions of the more
altruistic sex; Michener (110) has compiled sex ratios for social bees that seem
to support this argument. Such altruism could not affect primary sex ratios if it
occurred beyond the period of parental care (53), and were thus solely a matter of
kin selection.
The history of the situation in regard to sex of workers (and soldiers) is again
quite different in termites. Young termites are not helpless maggot-like offspring
tended from hatching to adulthood in cells as hymenopteran offspring were before
social behavior; termite sterility was not preceded by such extreme parental behav-
ior. And termite females evidently do not have the kind of immediate and precise
control over the sex ratio of their broods possessed by hymenopteran females.
Thus, to the extent that they are now extremely parental, male and female termite
workers probably became so more or less together.
A third point involves the production of males parthenogenetically by the
worker females. Some consider this tendency support for kin selection (60, p. 31),
some have considered it evidence against kin selection (101, pp. 153-55), and some
consider it evidence that offspring may evolve so as to compete directly against
their parents—in other words, they may “break out” of the clutches of manipula-
tive parents. But there are other ways to view this phenomenon, at least in some
cases. When a queen dies or is lost for whatever reason she has only one way to
reproduce further if there are no larvae that can still be made into queens. Her
final blaze of reproductive glory will be to have her workers make as many males as
they can before the colony is dead. I suggest that queens have been favored whose
workers begin frantically to make males with the slightest waning of her influence.
(Hamilton, 67, refers to such behavior by workers as “selfish,” apparently referring
to the “race” by the workers to see which will reproduce most. But such behavior
matches the mother’s wishes, and in some eusocial insects leads to the production
of a new queen, whereupon the workers “altruistically” kill the incipient queens
that didn’t make it).
The above explanation is insufficient to account for all of the varying reports on
the phenomenon of male production by workers (67, 101, 175); but, perhaps owing
to the fragmentary nature of current information, so is every other single explana-
tion. Perhaps more relevant than parent-offspring competition in the problem of
male production by workers is father-mother competition. Since all males are pro-
duced parthenogenetically, fathers will gain from producing both worker daugh-
ters that make males, in competition with their mothers, and, paradoxically, queen
daughters that do so while suppressing their worker daughters’ male production;
the effect through a male’s worker daughters is perhaps more immediate (see also
101). Queens, on the other hand, will gain from worker daughters that do not make
males and queen daughters that do and that suppress male production by their
worker daughters. When the queen is alive and healthy it is solely in the male’s
interest that worker females make sons, and this may be the only clear competition
86 { General Foundations

between male and female parents in colonies of social Hymenoptera. Coupling

this conflict with the value to the queen of her daughters making males when she
is dead or waning may provide explanations for many of the confusing variations
reported in this phenomenon. Moreover, a mechanism can be postulated whereby
the male may to some extent compete successfully against his mate in this regard;
this by constantly evolving sperm that are somehow able to thwart tendencies by
the queen to lay unfertilized eggs, while producing daughters that tend to lay if
they are phenotypically channeled into becoming workers.
The three points outlined above all seem to support the idea that the parents
of sterile insects have made them so in their own interests, and have made them
altruistic beyond the possibilities of kin selection as so far formulated. This the-
ory, which has not previously been proposed, is also supported by the fact that the
pheromonal influence of the queen is in every case either directly, or indirectly
through the existing castes, the determiner of sterility. And, as noted earlier, it
provides a solution to the question of why the queen honeybee has evolved a
special sting apparently used only against her sexual sister. Hamilton (67) was so
puzzled over this phenomenon as to suggest that Apis queens return from their
nuptial flight into strange colonies often enough for the queen’s sting to evolve as
a result. If the colony is largely a manipulation of the queen’s parental investment,
then both extremely altruistic and extremely selfish adaptations among offspring
are easily explained so long as they contribute to the queen’s reproduction. Not
only could a sting evolve solely because it efficiently dispatched the closest rela-
tive of the stinging individual at appropriate times, but the “quacking” of young
queens still in pupal cells, in answer to the “piping” of an emerged sister queen
whose response may be to sting them to death (68), can also be understood in
this light.
The queen’s sting, then, may be analogous to the necrotic tip of the proximal
embryo of the pronghorn, the graded sizes of owl nestlings, and the various other
determiners of clutch or litter size in different animals: it is a device that prevents
partitioning of the parental investment (measured in honeybees largely in terms
of available workers) beyond the point at which it is maximally reproductive to the
parent. That this circumstance is not clear from the arguments so far provided on
this topic (as Hamilton’s puzzlement would imply) indicates that it is insufficient to
argue that k in Hamilton’s (60) formula somehow includes variations in intensity
or directness of reproductive competition.
Obviously parental manipulation of progeny is not restricted to physical
coercion or pheromonal control. It means chiefly that parents with one kind of
offspring outreproduce those with another. Whether the offspring are selfish or
altruistic, and the exact manner in which they are caused to be selfish or altruistic,
is another problem. A good example with which to illustrate these points is the
paper wasp, Polistes fuscatus (68), often considered to represent an intermediate
stage in the evolution of sociality in insects because founding females are faculta-
tively sterile. One reason for its illustrative value is that founding females, which
 Parent-Offspring Conflict and Manipulation } 87

sometimes cooperate and may (frequently or always) be siblings, begin reproduc-

tion long after their mother’s death.
Queens of P. fuscatus begin nests in spring, build up a population of workers
during the summer, and in fall produce new queens and males. The new queens
both mate and overwinter apart from the old nest site. In spring they found nests
singly or in groups. When they found nests in groups only one queen lays, the oth-
ers serving as workers for her even though they too are fertilized. West-Eberhard
considered that the individual subordinates may gain genetically by cooperating
to help their most fit sister. But at least two potentially alternative explanations
exist and have not previously been discussed.
First, subordinate females may get to take over the nest (because the original
queen is somehow lost) often enough before the reproductive brood is produced.
(Production of queen daughters only near the end of summer after producing solely
diploid worker females also raises interesting questions about the fate of sperm
provided by different males). Second, queens may gain by producing daughters
that sometimes cooperate at the individual expense of all but the dominant, actual
queen and thus build fewer nests more swiftly. Obviously the old queen need not
be present at nest-founding for this altruistic tendency to evolve. Whether such
altruism evolves depends solely on whether the parents carrying the genes respon-
sible for it outreproduce. This outcome in turn will depend chiefly on two things:
1. Is it more reproductive to build fewer nests more swiftly? or 2. Is there a high
likelihood that subordinates will accidentally direct their altruism at nonsiblings?
If new queens tend to return to the old nest site to start nests, altruism may rarely
be misdirected. If they generally nest in new sites the possibility for error may be
increased. A testable difference in predictions is thus provided between the behav-
ior of individuals either of the same species or of different species with different
dispersing tendencies; unfortunately, without consistent differences in inbreeding
coefficients or number of matings per queen between populations it will not help
us in this case to distinguish between kin selection and parental manipulation.
We may ask, finally, why the sterility of subordinate Polistes queens remains
facultative. If the old queen is really producing, in effect, a brood of queens and
workers, why not obligate sterility? Three categories of environmental uncertainty
may combine to help explain this situation: 1. varying queen mortality or inca-
pacity before production of the sexual brood in autumn, 2. varying availability of
nest sites, and 3. varying likelihood of siblings reliably nesting together without
interlopers. Sometimes, apparently, the queen gains if all her surviving daughters
found nests alone.

Literature Cited

2. Alexander. R.D. 1961. Aggressiveness, territoriality, and sexual behavior in field crickets
(Orthoptera: Gryllidae). Behaviour 17:130–223.
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11. Altmann, S. A., Altmann, J. 1972. Baboon Ecology. African Field Research. N.Y.: Karger.
vii+220pp.
27. Brown, J. 1970. Cooperative breeding and altruistic behavior in the Mexican Jay
(Aphelocoma ultramarina s). Anim. Behav. 18:366–78
28. Brown, J. 1972. Communal feeding of nestlings III the Mexican Jay (Aphelocoma uttra-
marina): interflock comparisons. Anim. Behav. 20:305–403
41. Darwin, C. 1967. On the Origin of Species. A Facsimile of the first Edition with an
Introduction by Ernst Mayr. Boston: Harvard Univ. Press. xviii + 502 pr. Orig. Publ. 1859
50. Eberhard, W. G. 1972. Altruistic behavior in a sphecid wasp: Support for kin-selection
theory. Science 172: 1390–91
53. Fisher, R. A. 1958. The Genetical Theory of Natural Selection. N.Y.: Dover. xiv +291 pp.
60. Hamilton, W. D. 1964. The genetical evolution of social behaviour. I. II. J. Theor. Biol.
7:1–52
67. Hamilton, W. D. 1972. Altruism and related phenomena, mainly in the social insects.
Ann. Rev. Ecol. Syst. 3:193–232
68. Hansson, A. 1945. Lauterzeugung und Lautauffassungersvermögen der Bienen. Opusc.
Entomol. Suppl. 6:1–124.
75. Horn, H. S. 1971. Social behavior of nesting Brewer’s Blackbirds. Condor 72:15–23.
83. Kerr, W. F., Nielsen, R. A. 1967. Sex determination in bees (Apinae). J. Apicult. Res. 6:3–9
101. Lin, N., Michener, C. D. 1972. Evolution of sociality in insects. Quart. Rev. Biol. 47:131–59
109. Michener, C. D. 1958.The evolution of social behavior in bees. Proc. Tenth Int. Congr.
Entomol. Montreal 2:441–447
110. Michener, C. D. 1969. Comparative social behavior of bees. Ann. Rev. Entomol.
14:299–342
124. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in insects.
Biol. Rev. Cambridge Phil. Soc. 45:525–67
135. Rothenbuhler, W. 1957. Diploid male tissue as new evidence on sex determination in
honeybees. J. Hered. 48:160–68
152. Taber. S. 1955. Sperm distribution in the spermathecae of multiple-mated queen honey-
bees. J. Econ. Entomol. 48:522–25
158. Trivers, R. L. Haplodiploidy and the evolution of the social insects. Manuscript
159. Trivers. R. L., Willard. D. E. 1973. Natural selection of parental ability to vary the sex
ratio of offspring. Science 179:90–92
165. Webb, L.J., Tracey, J.G., Haydock, K. P. 1967. A factor toxic to seedlings of the same
species associated with living roots of the non-gregarious subtropical rain forest tree
Grevillea robusta. J. Appl. Ecol. 4, 13–25
166. West, M. J. 1967. Foundress associations in polistine wasps: Dominance hierarchies and
the evolution of social behavior. Science 157:1584–85
168. West-Eberhard, M. J. 1969. The social biology of polistine wasps. Univ. Mich. Mus. Zool.
Misc. Publ. 140:1–101
169. West-Eberhard. M.J. Toward an evolutionary theory of social behavior. Quart. Rev.
Biol. In press.
171. Williams, G. C. 1966. Adaptation and Natural Selection. Princeton, N.J.: Princeton Univ.
Press. x + 307 pp.
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173. Williams, G. C., Williams. D. C. 1957. Natural selection of individually harmful social
adaptations among sibs with special reference to social insects. Evolution 11:32–39
174. Wilson, E. O. 1963. The social biology of ants. Ann. Rev. Entomol. 8:345–68
175. Wilson, E. O. 1971. The Insect Societies. Cambridge, Mass.: Belknap. ix +548 pp.
178. Woyke. J. 1963. Drone larvae from fertilized eggs of the honeybee. J. Apicult. Res.
2:19–24
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PART } II

Human Social Evolution

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5}

Biology and Culture

In the beginning it was, “Why?”

curious, incredulous, or snickering.
And the answer came, quick and confident,
amid a swelling flood of pride.
And later there were no whys,
but respect, envy, association coveted.
Or perhaps the why was lost in a sea of shame
and smug, knowing nods –
no whys because they know now.
They know now!
And so it is I who wonders,
and the question bores, insistent,
and will not likely be answered.
Are the understanding and culture of all of ourselves
no more than feeble, stumbling fingers that
rip and tear in fruitless efforts to unravel
the complex fabric of cause and effect,
the too-intricately woven threads of truth?
Alexander, 2011, p. 22
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 INTRODUCTION
Mark Flinn, University of Missouri

I do not know what Richard Alexander dreams about. But when he is awake, he
seems endlessly driven to understand the most perplexing, difficult, important
questions about the evolution of life. Like Kipling’s Dingo running after Old Man
Kangaroo, the chase is always on. Of all the scientific enigmas that captured Dick’s
persistent, dogged attention, the evolutionary foundation for human culture is
perhaps best beloved1 with major discussions in many of Alexander’s articles and
in both Darwinism and Human Affairs (1979a) and The Biology of Moral Systems
(1987). His article “Evolution and Culture” in the classic volume Evolutionary
Biology and Human Social Behavior (edited by Napoleon Chagnon and William
Irons) is perhaps his singular most direct treatment of this difficult topic. It begins
with a stark line-in-the-sand:
. . . all of life is subjected continually and relentlessly to a process of differential
reproduction of variants . . . all of the aspects of life are owing, directly or indi-
rectly, to the cumulative effects of this process. No significant doubt has ever been
cast on the first part of this argument, and the only alternatives to the second,
advocated since 1858, have been divine creation and culture. (R.D. Alexander
1979b: 59)
This is a bold challenge. Is culture explicable as an outcome of the organic evo-
lutionary process, or is Culture something else, a separate and in some respects
independent process more akin to divine creation? The question remains unre-
solved; most of Alexander’s arguments are as salient today as they were over
30 years ago. In this introductory essay I summarize his key points about culture
and try to push the chase on by examining the issue of why human culture can
involve such astonishing levels of informational creativity.
Alexander starts by explaining several misconceptions and obstacles to under-
standing modern evolutionary theory. First he addresses the basic challenges

1
Among my childhood memories are the wonderful times spent snuggled together with my sib-
lings in front of a fireplace in my father’s study listening to bedtime readings. One of our favorites was
Kipling’s “Just-so” stories. That the label was later used by S.J. Gould and others as a derogation of
evolutionary analyses of human behavior seems small-minded. My own children prefer Alexander’s
books “Thumping on Trees” (2010) and “Red Fox” (2004) to Kipling.
96 { Human Social Evolution

Table 1 } Murdock’s Organic/Cultural Evolutionary Scheme

Evolutionary Processes Biological Cultural

Inheritance; information Gene (DNA) Culture trait (idea; meme)

Source of novel variation Mutation Innovation; mistakes
Selection Natural selection Choice
Mode of transmission Reproduction (genetics) Social learning
Random effects Drift Sampling error
Separation/contact Isolation/gene flow Cultural diffusion

posed by those who deny that “microevolutionary” (small, cumulative) changes

can produce major structures of organisms (such as the human brain) and dif-
ferences among species. Creationists posit that the “macroevolutionary” gaps
between humans and other life require divine intervention. Alexander notes that
exceptions to Darwin’s challenges (ways to falsify the general theory of evolution
by natural selection) have yet to be found (see also Alexander 2012).
On the other end are those that accept the general proposition that humans are
products of organic evolution, but see Culture as a distinct phenomenon, with its
own evolutionary processes. George Peter Murdock (1949) described an analo-
gous evolutionary scheme (table 1).
Alexander points out several key shortcomings of this analogy. First, it is not
clear that the units of cultural inheritance have the necessary property of high-
fidelity replication. “Genes” (DNA strands) can make exact physical copies of
themselves; ideas and mental representations do not have a similar consistent basis
for replication. Second, cultural innovations or inventions are usually directed at
solving problems and are not random in the sense that mutations are. The remark-
able creativity of human behavior is a special case that I examine more extensively
below. Third, and most important, the cognitive mechanisms (brain; mind) that
underpin cultural information are themselves products of human evolutionary
history. Hence cultural evolution is not independent of organic evolution (see
Alexander 1979:73).
Vygotsky (1978) observed that children are especially tuned to their social
worlds and the information that it provides. Alexander posits a complementary
adaptive logic: The social world is a rich, vital source of useful information for
cognitive development. The human brain has been designed by natural selection
to take advantage of this bonanza of data. Some, perhaps in a gesture of appease-
ment to the cultural tabula rasa old guard, would have culture running off in its
own (second) evolutionary system with its own distinct (but linked!) inheritance
mechanisms similar to Murdock’s scheme above (for reviews, see Dawkins, 1982;
Durham, 1991; Henrich & McElreath, 2003; Richerson & Boyd, 2005). Others
advocate a more restrictive grounding in the biology of learning (Tomasello,
2011), viewing socially learned information or culture as a rather special type of
phenotypic plasticity (Alcock, 2005; Flinn, 1997; Flinn & Alexander, 1982, 2007).
 Biology and Culture } 97

Alexander exemplifies this latter paradigm, modeling culture as a compilation of

flexible responses by individuals to specific environmental contingencies, analo-
gous to the biological concept of reaction norms and consistent with the basic
premises of evolutionary psychology (e.g., Daly & Wilson, 1983).
Here I examine how the Alexander model of culture goes beyond the con-
cept of “evoked culture” as constrained response to variable environments
guided by specialized psychological modules. Advances in the understanding
of the evolutionary basis of the phenotype, captured in part by the emergent
field of “evo-devo” (evolutionary developmental biology) and its reemphasis of
the complexity of ontogeny (West-Eberhard, 2003), have apparent relevance to
this question of culture and its variants (e.g., Frankenhuis & Panchathan 2010;
Heyes, 2003).
Alexander suggests that culture may be viewed as a highly dynamic information
pool that is generated and filtered by the extensive information-processing abili-
ties associated with our flexible communicative and sociocognitive competencies
(Alexander, 1979b). With the increasing importance and power of information
in hominin social interaction, culture and tradition may have become an arena
of social cooperation and competition (Flinn, 2004; see also Baumeister, 2005;
Sternberg & Grigorenko, 2004). The key issue is novelty. One of the most difficult
challenges to understanding human cognitive evolution, and its handmaiden cul-
ture, is the unique informational arms race that underlies human behavior. The
reaction norms posited by evolutionary psychology to guide evoked culture within
specific domains may be necessary but insufficient. The mind does not appear lim-
ited to a predetermined Pleistocene set of options—such as choosing mate A if in
environment X but choosing mate B if in environment Y—analogous to examples
of simple phenotypic plasticity, such as the development of winged and wingless
morphs in response to crowding and food availability in migratory locusts. The
human jukebox does not just keep the same old selection of tunes; the Beatles
displaced Elvis, and so forth. Humans do not have a limited, predetermined set of
phenotypic trajectories. We build airplanes.
Keeping up in the hominin social chess game required imitation. Getting ahead
favored creativity to produce new solutions to beat the current winning strategies.
Random changes, however, are risky and ineffective. Hence the importance of cog-
nitive abilities to hone choices among imagined innovations in ever more complex
social scenarios. The theater of the mind that allows humans to “understand other
persons as intentional agents” (Tomasello, 1999, p. 526) provides the basis for the
evaluation and refinement of creative solutions to the never-ending novelty of the
social arms race. This process of filtering the riot of novel information generated by
the creative mind favored the cognitive mechanisms for recursive pattern recogni-
tion in the open domains of both language (Deacon, 1997; Pinker, 1994) and social
dynamics. The evolutionary basis for these psychological mechanisms underlying
culture appears rooted in a process of “runaway social selection” (Alexander, 2006;
Flinn & Alexander, 2007; Flinn 2011).
98 { Human Social Evolution

Runaway Social Selection

Darwin (1871) recognized that there could be important differences between (a)
selection occurring as a consequence of interaction with ecological factors such
as predators, climate, and food, and (b) selection occurring as a consequence of
interactions among conspecifics (i.e., members of the same species competing
with each other over resources such as nest sites, food, and mates). The former is
termed natural selection and the latter social selection, of which sexual selection
may be considered a special subtype (West-Eberhard, 1983). The pace and direc-
tions of evolutionary changes in behavior and morphology produced by these two
types of selection—natural and social—can be significantly different (Alexander,
1974, 2005; West-Eberhard, 2003).
Selection that occurs as a consequence of interactions between species can
be intense and unending, for example with parasite–host red queen evolution
(Hamilton, Axelrod, & Tanese, 1990). Intraspecific social competition may generate
selective pressures that cause even more rapid and dramatic evolutionary changes.
Decreasing constraints from natural selection, combined with increasing social
competition, can generate a potent runaway process. Human evolution appears
characterized by such circumstances (Alexander, 2006; Flinn, Geary, & Ward,
2005). Humans, more so than any other species, appear to have become their
own most potent selective pressure via social competition involving coalitions
(Alexander, 1989; Geary & Flinn, 2001, 2002; Wrangham, 1999; e.g., Chagnon,
1988) and dominance of their ecologies involving niche construction (Deacon,
1997; Laland, Odling-Smee, & Feldman, 2000).
The primary functions of the most extraordinary human mental abilities—
language, imagination, self-awareness, empathy, Theory of Mind (ToM), foresight,
and consciousness—involve the negotiation of social relationships (Adolphs, 2003;
Flinn et al., 2011; Geary, 2005; Siegal & Varley, 2003; Tulving, 2002). The multiple-
party reciprocity and shifting nested subcoalitions characteristic of human sociality
generate especially difficult information-processing demands for these cognitive
facilities that underlie social competency (Flinn et al., 2012). Hominin social com-
petition involved increasing amounts of novel information and creative strategies.
Culture emerged as an increasingly potent selective pressure on the evolving brain.

Evolution of the Cultural Brain

The human brain is a big evolutionary paradox. It has high metabolic costs, it
takes a long time to develop, it evolved rapidly, it enables behavior to change
quickly, and it generates unusual levels of informational novelty. As noted earlier,
its primary functions include dealing with other human brains (Adolphs, 2003;
Gallagher & Frith, 2003). The currency is not foot-speed or antibody production
but the generation and processing of data in the social worlds of the human brains’
 Biology and Culture } 99

own collective and historical information pools. Some of the standout features of
the human brain that distinguish us from our primate relatives are asymmetrically
localized in the prefrontal cortex, including especially the dorsolateral prefrontal
cortex and frontal pole (Rilling & Sanfey, 2011; for review see Geary, 2005). These
areas appear to be involved with “social scenario building” or the ability to “see
ourselves as others see us so that we may cause competitive others to see us as
we wish them to” (Alexander, 1990, p. 7) and are linked to specific social abili-
ties such as understanding sarcasm (Shamay-Tsoory, Tomer, & Aharon-Peretz,
2005) and morality (Moll, Zahn, de Oliveira-Souza, Krueger, & Grafman, 2005).
An extended childhood seems to enable the development of these necessary social
skills (Flinn, Ward, & Noone, 2005; Joffe, 1997). Learning, practice, and experience
are imperative for social success. The information-processing capacity used in
human social competition is considerable and perhaps significantly greater than
that involved with foraging skills (Roth & Dicke, 2005).

Evolution of the Cultural Child

The altricial (helpless) infant is indicative of a protective environment provided

by intense parental and alloparental care in the context of kin groups (Alexander,
1990; Chisholm, 1999; Flinn & Leone, 2006; Hrdy, 2005; Muehlenbein & Flinn
2011). The human baby does not need to be physically precocial. Rather than
investing in the development of locomotion, defense, and food acquisition sys-
tems that function early in ontogeny, the infant can work instead toward build-
ing a more effective adult phenotype. The brain continues rapid growth, and the
corresponding cognitive competencies largely direct attention toward the social
environment. Plastic neural systems adapt to the nuances of the local community,
such as its language (Bjorklund & Pellegrini, 2002; Bloom, 2000). In contrast to
the slow development of ecological skills of movement, fighting, and feeding, the
human child rapidly acquires skill with the complex communication system of
human language (Pinker, 1999). The extraordinary information-transfer abilities
enabled by linguistic competency provide a conduit to the knowledge available in
other human minds. This emergent capability for intensive and extensive commu-
nication potentiates the social dynamics characteristic of human groups (Deacon,
1997; Dunbar, 1997) and provides a new mechanism for social learning and culture.
The recursive pattern recognition and abstract symbolic representation central to
linguistic competencies enable the open-ended, creative, and flexible information-
processing characteristic of humans, especially of children.

Reconciling Domain-Specific Modularity with Informational Novelty

Humans are unique in the extraordinary levels of novelty that are generated by
the cognitive processing of abstract mental representations. Human culture is
100 { Human Social Evolution

cumulative; human cognition produces new ideas built on the old. To a degree
that far surpasses that of any other species, human mental processes must contend
with a constantly changing information environment of their own creation.
Cultural information may be especially dynamic because it is a fundamen-
tal aspect of human social coalitions. Apparently arbitrary changes in cultural
traits, such as clothing styles, music, art, perceptions of beauty, food, dialects, and
mate choice decisions, may reflect information “arms races” among and within
coalitions.
The remarkable developmental plasticity and cross-domain integration of
some cognitive mechanisms may be products of selection for special sensitivity to
variable social context (e.g., Boyer, 1998; Carruthers, 2002; Sperber & Hirschfeld,
2004). Human culture is not just a pool or source of information; it is an arena
and theater of social manipulation and competition via cooperation. Culture is
contested because it is a contest.
The effects of coalition conformity and imitation of success may drive cul-
ture in directions difficult to predict solely on the basis of simple functional con-
cerns or evolved psychological mechanisms. This social dynamic would explain
the apparent lack of a simple biological utilitarianism of so much of culture and
the great importance of historical context and social power (e.g., Wolf, 2001).
Deconstruction is a complicated but necessary enterprise, for we are all players in
the social arena. The twist is that we are evolved participants.
Alexander’s analysis of culture may reconcile important gaps between the evo-
lutionary psychological paradigm and the more history-oriented anthropological
approaches (e.g., Richerson & Boyd, 2005) because it suggests an evolved human
psychology that is creative, dynamic, and responsive to cultural context, rather
than being more rigidly constrained by domain-specific modules, or by an inde-
pendent system of cultural rules.
Understanding the evolutionary basis for human culture is far more than a
difficult academic issue. Such an understanding is critical to solving humanity’s
great problems of environmental degradation, social injustice, overpopulation,
and war. Alexander’s ideas about culture have become increasingly influen-
tial and broadly accepted, and continue to provoke deeper analyses of how the
human mind evolved in concert with an increasingly complex informational
environment.

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 EVOLUTION AND CULTURE 1
Richard D. Alexander

Excerpt from Evolutionary Biology and Human Social Behavior (N.A. Chagnon
and W. Irons, Eds.), 1979, Duxbury Press, North Scituate, MA: Duxbury Press,
pp. 59-85.
The basic argument developed by Darwin, and destined to become the cen-
tral principle upon which all of biology rests, was two-part in nature. The first
part was that all of life is continually and relentlessly subjected to a process
of differential reproduction of variants, which Darwin termed natural selec-
tion or “survival of the fittest.” The second was that all of the attributes of life
are owing, directly or indirectly, to the cumulative effects of this process. No
significant doubt has ever been cast on the first part of this argument, and
the only alternatives to the second, advocated since 1859, have been divine
creation and culture.

Debates over the Scope of Selection

CONCERNING DIVINITY

The effects of accepting both parts of Darwin’s argument are that (1) the traits
of modern organisms are, in terms of the environments of history at least,
assumed to be means of maximizing genetic reproduction and (2) the patterns
of long-term change observable from paleontological data are assumed also
to be owing to natural selection. Creationists believe that unfilled gaps in the
paleontological record imply creation, hence did not involve change by natural
selection; and most thoughtful people would agree that some extensive changes
during human history, evidenced in the archaeological record, are likely to have
been unaccompanied by genetic change, hence also did not involve change by
natural selection.
A degree of importance for natural selection has been granted by both cre-
ationists and the most radical adherents to the idea that culture and biology have

1
I thank Laura Betzig for allowing me to read an essay of hers which prompted me to begin imme-
diately to develop and write down some of the ideas in this paper.
 Biology and Culture } 105

been independent throughout human history. Thus, the organized supporters of

creation as an alternative to evolution, such as members of the Creation Research
Society (see the Creation Research Society Quarterly), have found it necessary to
accept the process of natural selection, which they refer to as “microevolution”
(e.g., Moore and Slusher 1970). They have established their line of defense chiefly
against “macroevolution,” which is their name for natural processes, supposed
by others to account for the formation of “major organs” and for the origin of
large changes or differences among organisms, such as exist between species
or “major groups.” The creationists argue that because the formation of major
groups or major organs cannot be observed directly or studied by experiment,
its analysis is outside science; and they argue that this process is best explained
as creation. Understandably, they have remained indefinite about the precise
nature of major groups and major organs, or the levels at which divine creation
is unavoidable.
Many lines of evidence indicate that creationists are wrong in their efforts
to distinguish long-term and short-term changes in evolution. Darwin offered
a devastating critique of this view, and anticipated the small, cumulative effects
of gene mutations as well, when he noted that major organs are the products of
large numbers of small changes of the observable kind attributed by creationists
to “microevolution.” This fact is easily demonstrated by crossing organisms with
variant forms of a given major organ or attribute. Darwin went so far as to offer the
challenge that “If it could be demonstrated that any complex organ existed, which
could not possibly have been formed by numerous, successive, slight modifica-
tions, my theory would absolutely break down” (1967[1859]:189). A related class
of evidence derives from laboratory or forced hybridization of different species or
genera, a procedure which clearly shows that differences between such forms are
also accumulations of small mutational changes of the directly observable kind
(see also Alexander, 1978b).

CONCERNING HUMANITY

Creationists thus deny that the second part of Darwin’s thesis applies to humans
by denying that the earliest of human attributes—i.e., those actually responsible
for the designation “human”—originated through natural selection. Students of
culture, on the other hand, tend to deny that the most recent of human attributes
can be understood by reference to natural selection—i.e., the details of cultural
patterns and differences—because they feel that the advent of traditionally trans-
mitted learning signaled the end of any necessary relationship between behavior
and the differential reproduction of alternative genetic elements.
Some recent authors have developed arguments, often explicitly about human
behavior and culture, as alternative to natural selection in ways that may seem to
cast doubt upon even the first part of Darwin’s argument. Three such arguments
seem most prominent.
106 { Human Social Evolution

Is Selection Tautological?
The first argument is that the basic thesis of natural selection is tautological.
Supporters of this view (e.g., Peters 1976) contend that we are unable to identify
the “fittest” organisms or traits except retrospectively, and that, accordingly, we
can only identify them as those which have survived. This argument ignores an
enormous body of evidence confirming its falsity. Biologists, as well as plant and
animal breeders, are continually able to identify as unfit individual organisms
whose phenotypic attributes reveal ahead of time that their chances of reproduc-
ing are either nonexistent or relatively small (see also Ferguson 1976; Stebbins
1977). Success in such predictions is possible, as with the maintenance of adapta-
tion, only to the extent that environments are predictable. But all environments
of life have some predictable aspects. We can prove this directly, and the count-
less fashions in which organisms are marvelously and intricately tuned to their
environments show that we are correct in assuming that the empirical evidence
of environmental consistency is relevant to the process of evolution. Modern
evolutionary biology depends upon an ability to generalize about adaptiveness,
both across genetic lines and across generations, and remarkable success is being
realized from such generalizations, especially with attributes common to most or
all organisms, like sex ratios, senescence, and parental investment, and others for
which the social environment is crucial, like group-living, nepotism, and sexual
competition (see references in Alexander 1977a, 1977b, and Alexander et al., this
volume, chapter 15). In the first case more effective comparisons are possible; in
the second, the winning strategies are more stable and more easily identifiable.
Criticisms that statements about natural selection are tautological only concern
their predictive value, but some detractors have supposed that they also cast into
doubt the existence or universality of the entire process. Even retrospective judg-
ments, however, are entirely sufficient to demonstrate the inevitability of differen-
tial reproduction, whether or not humans are aware of its workings or capable of
assessing its consequences.
The argument that natural selection is tautological is often linked with state-
ments by prominent evolutionists, such as Mayr (1963) or Simpson (1964), that
evolution is not a particularly predictive or predictable phenomenon, to suggest
that evolution does not even qualify as a scientific theory. The misapprehension
involved is failure to see that Simpson and Mayr were talking about our inability to
predict or give the adaptive reasons for ancient or long-term phylogenetic changes
because we are necessarily ignorant of the environments of selection during geo-
logical time. We are not so ignorant of the current and recent environments of
selection, and our understanding of them grows constantly.
Organic evolution leads to patterns of change in morphology, physiology, and
styles of life. Some of these patterns are reflected by fossil remains and some by
the array of organisms present at any given time. Evolution also involves spe-
ciation, which results in irreversible divergences of different patterns of life.
Pattern changes and speciation together lead to phylogenies or family trees that
 Biology and Culture } 107

presumably, if the record were complete, could be reconstructed to illustrate the

whole history of life. But phylogenetic patterns, although they are outcomes of
evolution, are not the essence of the process. The essence of the process is differ-
ential reproduction, or, as Williams (1966) put it, the maintenance of adaptation.
Phylogenies are reconstructed with little understanding of the selective forces
that produced their patterns because the environments of long-term history can-
not be reconstructed with the precision necessary to reconstruct the generation-
by-generation effects of natural selection. Efforts to “predict” phylogenies, or the
nature of species (i.e., to presage what will be discovered about either the past or
the future when more complete information is available) fail to the extent that
we are ignorant about environments and the array of living organisms present
at each time and place in history. They do not fail, as Peters (1976) suggested,
because of the demonstrable independence between the causes of mutations and
the causes of selection. Our inability to make long-term evolutionary predictions
thus does not mean that the nature of the process yielding evolutionary patterns
is itself to be doubted, or that evolutionary propositions are so tautological as to
fail as scientific theory. Predictions about adaptiveness are most accurate when
they concern short-term changes in the present, and there is every reason to
believe that they fail increasingly with longer time spans, or when other eras are
considered, simply because our information about environments is more incom-
plete in such cases.
Arguments about the relationship of long-term pattern changes during evolu-
tion to the process of natural selection, which is widely accepted as responsible for
short-term changes, have relevance here because of the common failure to real-
ize that long-term pattern-tracing (paleontology, archaeology) can be carried on
without direct attention to or concern for the process responsible. In biologists’
terms, the process of change is guided largely by natural selection. For anthropolo-
gists, it is probably fair to say that there is no universally accepted guiding force to
account for the changes commonly called cultural evolution or for modern varia-
tions in culture. The question we must ultimately address is: what is the nature of
this guiding force and to what extent has it been the differential reproduction of
genes, realized through reproductive striving of individuals? In this question there
is no implication that reproductive striving is consciously so directed.

Is Selection Often Impotent Because of Lack of Genetic Variation?

The second argument seeming to cast doubt on the universality of natural selec-
tion is that genetic variations relevant to selective forces are not always pres-
ent, rendering selection ineffective. But this argument only specifies rare and
temporary situations. As any plant or animal breeder knows, even in genetic
lines on which directional selection has been practiced for a very long time,
genetic variants and combinations now and then appear which are relevant to
a desired direction of change. Because of their unpredictability, the only way to
take advantage of such variants is to maintain selection. This realization causes
108 { Human Social Evolution

humans to practice artificial selection in a way that parallels the differential

reproduction of organisms induced by natural environments, which is also inex-
orable whether or not the variations involved are heritable (and also ineffective
when they are not).
For this reason we may assume that in natural populations most novel variants
which increase reproduction spread and become characteristic of the population,
and that this is the usual process of evolutionary change.
The reasons why natural selection is regarded as the guiding force of evolution
are not commonly discussed, but they are obviously crucial (see Alexander 1977a,
for a fuller discussion). The most apparent ones are the following: (1) altering direc-
tions of selection alters directions of change in organisms (probably always, even if
there is sometimes delay owing to specialization as a result of previous selection),
(2) the causes of mutation (chiefly radiation) and the causes of selection (Darwin’s
“hostile forces” of food shortages, climate, weather, predators, parasites, and dis-
eases) are independent, (3) only the causes of selection remain consistently direc-
tional for relatively long periods (thus, could explain directional changes), and (4)
predictions based on the assumption that adaptiveness depends solely on selec-
tion are met (e.g., consider the history of sex-ratio selection: Fisher 1958[1930];
Hamilton 1967; Trivers and Willard 1973; Trivers and Hare 1976; Alexander and
Sherman 1977; Alexander et al., Chagnon et al., this volume).
The greatest constraints on selection occur then, paradoxically, in two opposite
situations: when the change of selective direction is very great and when unidirec-
tionality persists for a very long time. In the first case, specializations as a result
of previous selection reduce the likelihood of adaptive changes in certain direc-
tions; thus, moles are almost certainly less likely than squirrels to evolve wings.
In the second case, alleles causing change in the favored direction are apt to be
fixed by selection faster than mutants arise; thus, after generations of selection for
increased milk production, dairy farmers know that “management” (i.e., environ-
ment) is crucial but, obviously, they will continue to favor breeding stock from
their best producers in the expectation that once in a while the differences will
be heritable. Unlike many aspects of phenotypes, cultural variations of humans,
which lack correlation with genetic variations, may nevertheless be heritable
because of traditional transmission of learned behaviors. Thus, as is well under-
stood, culture has the unusual property of being able to evolve cumulatively in
the absence of genetic change. Rates of cultural change within historical times are
clear evidence that massive cultural change does indeed occur without genetic
change, or in its virtual absence.
However, for cultural change to be independent of natural selection, the follow-
ing hypotheses would also have to be true: (1) because directions and rates of cul-
tural change are potentially independent of many or most human genetic changes,
they are independent of the history of natural selection upon humans; and (2)
genetic change through natural selection is not induced by cultural changes. Until
very recently, both of these hypotheses have remained largely untested; should
 Biology and Culture } 109

they eventuaIly be rejected, as I believe likely, then even for human culture the
second part of Darwin’s argument will stand as stated above.

Does Evolutionary Theory Suggest Genetic Determinism?

The third argument about the relationship of biology and culture is exempli-
fied by the newspaper announcement of the British Broadcasting Corporation
film “The Human Animal,” which identified sociobiology as “The field of study
built on the theory that behavioral patterns in humans are inherited through
genes.” This definition is, perhaps innocently, a version of the argument that
efforts to invoke biological explanations of human behavior are efforts to defend
the notion that behavior is “genetically determined.” It cannot be denied that
some statements by biologists also suggest this kind of naivete, But there is equal
naivete in supposing that merely to consider genes as influences upon behavior
(or any other aspects of phenotypes) means that one is automatically excluding
the environment or under-playing its role. To argue that behavior is a product of
a history of natural selection, however, is in no way an argument that behavior
is determined by the genes. It is almost the opposite—a declaration instead that
the behavior of each organism is determined, not by the genes, but by the genes
and the developmental and experiential environment together. That the mere
introduction of genes as influences on behavior is construed as an unsupport-
able kind of genetic determinism is indicated by the tendency to contrast expla-
nations which include genes with explanations invoking learning. For so many
years we asked: “Is this behavior learned or genetic?” Finally, we are coming
to realize that the answer is always “Both.” The consequence of this realization
is not the exclusion of biology from considerations about human behavior but
its appropriate reintroduction into them. (For fuller discussions see Alexander
1978a, 1977b, 1977c.)

Traits, Learning, and Genetic Variation

To explain this paradox it is fruitful to consider still another question recently
made prominent by self-professed critics of evolutionary approaches to the analy-
sis of human behavior. What is a “trait”? This question seemingly has two aspects.
First is the problem of how much or what part of the phenotype can be viewed
as a unit in terms of function. In other words, upon what parts and amounts of
the phenotype is selection acting in a given circumstance or environment? How
much of the phenotype does a given kind or aspect of selection affect? The second
part of the question involves how the genes work together during ontogeny to
create the phenotype—in other words, how do the genes in the genotype relate to
the identifiable components of the phenotype? A history of natural selection sug-
gests that in some sense these two problems resolve into a single one: How do the
units within genotypes (genes, supergenes, chromosomes, etc.) interact (through
epistasis, pleiotrophy, linkage, etc.) to produce the functional units (appendages,
sensory devices, reproductive organs, etc.) of the phenotype?
110 { Human Social Evolution

This question relates to the genes/learning dichotomy because of a common

confusion between (1) whether or not a particular behavioral variant charac-
terizes a particular genotypic variant and (2) whether or not a particular set of
behaviors characterizes a particular genotypic variant. If a particular behavioral
act was learned, then its individual presence as a variant is clearly not a result of
genetic variation. But genes are necessarily causal (together with their environ-
ment) in the production of all behavior; the only problem is to understand how.
To reach this understanding we must consider entire sets of learned behaviors
in the set of different individuals possessing the same set of genes influencing
that behavior in the collection of environments in which the set of individuals
developed. Ideally, such entire sets of learned behaviors would be compared with
other sets of learned behaviors in other sets of organisms which do differ geneti-
cally. In a species with a great deal of immediate-contingency learning in the
behavioral repertoires of individuals, then, the effects of genes on learned behav-
ior can only be understood by analyzing the behaviors expressed by numerous
individuals who collectively have experienced the array of environments in which
the behavior in question has evolved, or the environments in which it has usu-
ally been expressed. Traits can only be identified by examining the variations
in learned activities in the normal range of environments of learning. Genetic
change could shift the ease of learning in such a group of organisms one way or
another along one or more axes, or reduce or abolish certain possibilities. The
adaptive or evolved aspect of learning traits so identified will be the nature or
range of expression correlated with the usual environments of history, with non-
adaptive, maladaptive, or evolutionarily incidental aspects represented by those
appearing in novel or rare environments. Obviously, such “incidental” or non-
evolved aspects of learning are crucial in understanding human behavior because
of the extraordinarily rapid changes induced by culture and technology. What
would be left is a set of learning abilities, the range and relative ease of which have
been tuned by natural selection acting on the genetic makeup of the population.
It is difficult for me to conceive of any other relationship between learned behav-
iors and the process of natural selection.
Indeed, what I have just described is the general relationship between natu-
ral selection and all kinds of expressions of the phenotype, whether behavioral,
physiological, or morphological. This is the reason why—even though learning, or
variation resulting from environmental variation, is an explanation for observed
behavioral variations which is alternative to an explanation based on genetic
variation—cultural evolution is not an alternative to natural selection as a gen-
eral explanation for the nature of human activities. Cultural patterns are, like all
expressions of the phenotype, outcomes of different developmental environments
acting on sets of genetic materials accumulated and maintained by natural selec-
tion. Culture differs from other aspects of phenotypes in the degree to which it
can change without genetic change; but behavior in general differs from morphol-
ogy and physiology in the same regard. This is the raison d’etre of behavior. It is
 Biology and Culture } 111

a way of responding to a greater proportion of the information available to the

organism from immediate contingencies in its environments. Culture is a par-
ticular and elaborate system of behavior for doing the same. The questions we are
led to ask about culture, after considering it in a biological context, are the same
that would be asked from any other analytical approach: What forces influence
its patterns? What do its expressions mean? The only distinctive aspect of a bio-
logical approach is that we are apt to ask these questions in relation to biological
functions, or reproduction. This attitude may seem alien to social scientists, but
the correct answers to questions about the significance of culture will be the same
regardless of the manner in which they are approached.

CONCERNING CULTURE: NATURAL SELECTION AND CULTURE

THEORY

Probably because anthropologists and others tended to identify the possession of

culture and the capacity for culture as peculiarly human traits, the concept of cul-
ture has acquired and retained a certain singularity: hence, perhaps, efforts to seek
general or singular theories of culture; and perhaps also the assertion by inves-
tigators reluctant to see culture in this way that “Culture is dead”- that is, that it
does not possess the singularity attributed to it and that truly general theories
of culture are therefore unlikely. Others, still convinced about the generality of
the concept of culture, have come to the notion that, in the absence of acceptable
functional explanations, culture can only be explained in terms of itself, or as a set
of arbitrarily assigned meanings or symbolizations (White 1949; Sahlins 1976b),
and specifically cannot be explained in terms of utilitarianism of any sort or at any
level. White, for example, writes skeptically of man’s “vaunted control of civiliza-
tion” and of the fond belief that it “lies within man’s power... to chart his course as
he pleases, to mold civilization to his desires and needs.”
Culture, such authors seem to be arguing, is something greater than humans
collectively and almost independent of humans individually: It continues on
courses perhaps unpredictable, and certainly swayed but slightly by the wishes of
individuals, who are merely its “passive” transmitters. Sahlin; comes very close to
describing culture as an aspect of the environment of humans about which they
can do little but accept it in just those terms, thereby almost paralleling the biolo-
gists’ concept of the genotype and the phenotype as parts of the environment of
selection of the individual genes.
But, if human evolution, like that of other organisms, has significantly
involved selection effective at genic levels, realized through the reproductive
strivings of individuals, neither humans as individuals nor the human species
as a whole have had “a” course to chart in the development of culture but rather
a very large number of slightly different and potentially conflicting courses. In
such event it would indeed be difficult to locate “a function for,” or even “the
functions of,” culture; instead, culture would chiefly be, as Sahlins’ view may
112 { Human Social Evolution

be slightly modified to mean, the central aspect of the environment into which
every person is born and must succeed or fail, developed gradually by the col-
lections of humans that have preceded us in history, and with an inertia refrac-
tory to the wishes of individuals, and even of small and large groups. Culture
would represent the cumulative effects of inclusive-fitness-maximizing behavior
(i.e., reproductive maximization via all socially available descendant and non-
descendant relatives) of the entire collective of all humans who have lived. I here
advance this as a theory to explain the existence and nature of culture, and the
rates and directions of its change.
If this theory is appropriate, then aspects of culture would be expected to be
adversary to some of the wishes of each of us; few aspects of it would be viewed
with equal good humor by all of us; and in just this circumstance we would not
expect grand utilitarian views of culture, general theories of culture, or efforts at
purposeful guidance of culture to succeed easily. These are exactly the kinds of
failures that have always plagued culture theorists. Yet, by this theory, the inertia of
culture would exist because individuals and groups did influence its directions and
shape, molding it—even if imperceptibly across short time periods—to suit their
needs, thereby incidentally increasing the likelihood that subsequent individuals
and groups (a) could find ways to use it to their own advantages as well and (b)
could not alter it so greatly or rapidly.
It would also be a source of confusion, in attempts to relate directions and rates
of cultural change to utilitarian theories, that the reproductive efforts of individu-
als would not actually be directed at changing culture, as such; nor would such
efforts lead to any particular directions of change in culture as a whole. The striv-
ing of individuals would be to use culture, not necessarily by changing it, to further
their own reproduction. No necessary correlation would exist between success in
the reproductive striving of an individual and the magnitude of the individual’s
effect on cultural change, or between the collective success of the individuals mak-
ing up a group or society and the rate of cultural change. It would not matter if
one were a legislator making laws, a judge interpreting them, a policeman enforcing
them, a lawyer using them, a citizen obeying them, or a criminal circumventing
them: Each of these behaviors can be seen as a particular strategy within societies
governed by law, and each has some possibility of success.
Again, it would tend to be contrary to the interests of the members of society
that cultural changes of any magnitude could easily be effected by any individu-
als except for inventions seen as having a high likelihood of benefiting nearly
everyone. The reasons are that (1) changes, effected by individuals or subgroups
in their own interests, would likely be contrary to the interests of others; and (2)
once individuals have adopted and initiated a particular set of responses to the
existing culture around their own interests, changes of almost any sort have some
likelihood of being deleterious to them. These arguments not only suggest how
anthropological interpretations of culture may be entirely compatible with the
notion of reproductive striving principally effective at the individual (or genic)
 Biology and Culture } 113

level, but also may explain the genesis of views that culture is somehow indepen-
dent of individuals and groups and their wishes, and not easily explainable in
utilitarian terms.

The Evolution of Culture

It is a fundamental characteristic of culture that, despite its essentially

conservative nature, it does change over time and from place to place. Herein
it differs strikingly from the social behavior of animals other than man. Among
ants, for example, colonies of the same species differ little in behavior from one
another and even, so far as we can judge from specimens imbedded in amber,
from their ancestors of fifty million years ago. In less than one million years
man, by contrast, has advanced from the rawest savagery to civilization and
has proliferated at least three thousand distinctive cultures.
[george peter murdock, 1960b:247]
If long-term changes in human phenomena, as evidenced for example in the
archaeological record, are cultural, and were not induced by natural selection or
accompanied by genetic changes relating to cultural behavior, then we should
be interested in answering two questions: First, what has guided cultural evolu-
tion? What forces can account for its rates and directions of change? Second, what
degrees and kinds of correspondence exist today between the patterns of culture
and the maximization of genetic reproduction of the individuals using, transmit-
ting, and modifying culture? Are the degrees and kinds of correspondence, and of
failure to correspond, consistent with the forces presumed to underlie rates and
directions of cultural change?
At one end of a spectrum lies the possibility that all of the cultural changes
during human history have been utterly independent of genetic change, neither
causing such nor caused by it. At the other end is the possibility that changes in
human behavior have correlated with genetic change to approximately the same
degree as changes in the behavior of other species, such as non-human primates.
Observations within recorded history are sufficient to show that neither of these
extreme possibilities is likely. As examples, cultural changes, such as eyeglasses and
treatments for diabetes, obviously influence genetic change; and cultural changes
clearly have accelerated tremendously in recent decades without any evidence of
parallel acceleration in genetic change. At least, then, cultural changes do influ-
ence genetic change although there is apparently no clear evidence that genetic
changes are causing cultural changes, or that there is any close correlation between
cultural changes and genetic changes that specifically influence behavior in rela-
tion to culture. Now, it is easy to understand, on theoretical grounds, how culture
can change cumulatively without accompanying genetic changes that relate to the
behaviors involved-and easy to argue that numerous such changes have occurred
within recorded history when strikingly different cultures merged. Therefore the
114 { Human Social Evolution

significance of the above two questions about the forces which change culture
and the relationships of culture to maximization of reproduction by individuals
is brought into an even sharper focus. We expect that the answers to these two
questions will be complementary, and that the efforts to answer them should be
conducted simultaneously and jointly.
Some changes in culture, such as those influenced by climatic shifts, natural
disasters, and diseases, predators, and parasites (of humans and the plants and ani-
mals on which they depend), are beyond human control; others are explicitly under
such control, although such control may be very direct (invention and conscious
planning) or not so direct (resource depletion and pollution). The difficult ques-
tion, in understanding the relationship between culture and our inevitable history
of natural selection, is not in discovering the reasons behind cultural changes, as
such, which are actually fairly obvious. Instead, it is in understanding exactly how
such changes influence culture: What is done with them? What direction of change
do they induce, and why? Those changes in culture which are consequences of
human action appear to represent products of the striving of individuals and
groups of individuals. Such changes, as with extrinsically caused changes, are also
responded to by changes in the striving of individuals and groups of individuals.
Inventions are seized upon. Pollution and resource depletion are lamented, and
cause geographic shifts in population or efforts at inventions or practices which
will either offset their effects on the lives of those showing the effort or allow them
to take advantage of such effects. Attempts are made to predict and offset natural
disasters and climatic shifts. All of these responses are easily interpretable as part
of efforts by individuals, acting alone or in groups, to use culture to their own
advantage in the fashion already suggested. But culture is not easily explainable as
the outcome of striving to better the future for everyone equally: If that were the
case, then surely conscious planning would quickly become the principal basis
for cultural change, and it would be carried out with a minimum of disagreement
and bickering (perhaps we shall actually be able to make our interests coincide to
a greater degree by realizing that we have a background of competition in genetic
reproduction, which may be less interesting to us once exposed to our conscious
reflection).
It is possible to examine the problem of cultural change in a fashion parallel to
that used for evolutionary change (e.g., Alexander 1977a). We can ask about the
same five phenomena which characterize the process of genetic change (the most
closely parallel argument is probably that of Murdock [1960b]).
1. Inheritance: Just as the morphological, physiological, and behavioral
traits of organisms are heritable, given consistency in the developmental
environment, the traits of culture are heritable through learning. They may
be imitated, plagiarized, or taught.
2. Mutation: Like the genetic materials, culture is mutable, through
mistakes, discoveries, inventions, or deliberate planning (Murdock’s “varia-
tions,” “inventions,” and “tentations”).
 Biology and Culture } 115

3. Selection: As with the phenotypic traits of organisms, some traits of cul-

ture reinforce their own persistence and spread; others do not, and eventually
disappear for that reason (Murdock’s “social acceptance,” “selective elimina-
tion,” and “integration”). (See also Campbell 1965, 1975.)
4. Drift: As with genetic units, traits of culture can also be lost by acci-
dent or “sampling error.”
5. Isolation: As with populations of other kinds of organisms, different
human societies become separated by extrinsic and intrinsic barriers; they
diverge, and they may come into contact and remerge or continue to drift
apart; items and aspects of culture may spread by diffusion (Murdock’s “cul-
tural diffusion” and “cultural borrowing”).

Immediately, differences are apparent between the processes of change during

genetic and cultural evolution. Unlike genetic evolution, the causes of mutation
and selection in cultural evolution are not independent: Instead, there is a feed-
back between need and novelty. Most of the sources of cultural “mutation” are
at least potentially related to the reasons for their survival or failure. Some cul-
ture theorists have tended to deny utilitarian connections between the sources or
causes of cultural change and the reasons for their survival or failure. I suggest that
the reason for these denials is that such theorists have never sought function both
in terms of reproduction and at the individual level, as biologists now realize must
be the case in organic evolution. Some, such as Franz Boas and Ruth Benedict,
have emphasized the individual; others, such as Bronislaw Malinowski and A. R.
Radcliffe-Brown, have emphasized function as survival value—even, sometimes,
to the individual. None, however, has seen function as reproductive value. Instead,
most functionalists have either sought group-level utilitarian effects or have
regarded survival, not reproduction, of the individual as crucial (for reviews of
such views, see Hatch 1973; Harris 1968).
Some recent investigators, such as Cloak (1976), Dawkins (1976), Durham
(1976a), and Richerson and Boyd (1978), have concentrated on heritability of cul-
tural traits (or cultural novelties or “instructions”) and argued that their separate
mode of inheritance thwarts the operation of natural selection of genetic alter-
natives. I regard this approach to the history of culture as similar to a view of
the natural history of organisms that sees phenotypes in general (as opposed to
no phenotypes) as essentially thwarters of natural selection. In one sense they
are, since they necessarily render the action of selection on the genes less direct:
Selection must now act through the phenotype. But this change had to have
occurred because those genes that reproduced via phenotypes outsurvived their
alternatives in the environments of history. So must it be with the capacity for cul-
ture, as the above authors for the most part acknowledge. Even if culture out-races
organic evolution, creating blinding confusion through environmental novelties,
to view the significance of its changes and its traits as independent of, or as mere
thwarters of, natural selection of genetic alternatives, would be parallel to suppos-
ing that the function of an appetite is obesity.
116 { Human Social Evolution

The important question in cultural evolution is: Who or what decides which
novelties will be perpetuated, and how is this decided? On what basis are cultural
changes spread or lost? In other words, we are led to analyze exactly the same
part of the process of cultural change as for genetic change. In cultural change the
answer to this question of who decides, and how, actually determines the herita-
bility of culture, since heritability of cultural items at least theoretically can vary
from zero to 100 percent from one generation to the next, or even within genera-
tions. Any cultural trait, unlike a gene, theoretically can be suddenly cancelled
and just as suddenly reinstated, in the population as a whole. Again, in theory
at least, this can be done as a result of conscious decision based on what the
involved parties see as their own best interests at the time. This reinforcing rela-
tionship among selection, heritability, and mutation in culture means that, unlike
organic evolution, heritability of culture traits will not be steadily increased; nor
will mutability be depressed because the majority of mutations are deleterious in
the individuals in which they arise owing to the lack of feedback between muta-
tional directions and adaptive value. Some cultural mutations appear (that is, are
implemented, or translated from thought to action) because they are perceived
to have value. Unlike evolutionary change, then, cultural change will acquire
inertia to the extent that the interests of individuals and subgroups conflict (and
have a history of conflicting), and whenever the distribution of power is such as
to result in stalemates. In part this means that cultural change may be expected
to continue accelerating, and this acceleration, I believe, will not only make it
increasingly difficult to interpret human behavior in terms of history, but will also
increasingly become apparent as the source of novel ethical problems, bound to
increase in numbers and severity as cultural change accelerates, because ethical
problems derive from conflicts of interest and these are bound to become more
complex (Alexander, 1979).
Most recent and current efforts to relate genetic change and cultural change,
then, seem really to be efforts to divorce them - to explain why and how culture
and genes came “uncoupled” during human history. These arguments generally
assume that the uncoupling is essentially synonymous with the appearance of
culture—that culture is, by definition, an uncoupling of human behavior from
gene effects.
I think these are the reasons why virtually all efforts to understand culture in
biological terms have failed. We can easily assume that the capacity for culture
allowed (as an incidental effect) various degrees of uncoupling of human behav-
ior from reproductive maximization. In modern urban society, for example, such
uncoupling is rampant. But to assume that uncoupling is the (historical, biologi-
cal, evolutionary) function of culture, or its basic significance or attribute, is, as
already suggested, like assuming that the function of an appetite is obesity.
There is enough evidence, even in everyday life, to indicate that in general
human social behavior is remarkably closely correlated to survival, well-being,
and reproductive success. If one accepts this assumption then it is easy to agree
 Biology and Culture } 117

that the real question is: What forces could cause the continued coupling between
culture and genes? In effect, we must discover, for cultural as well as genetic evo-
lution, the nature of the “hostile forces” (paralleling Darwin’s “Hostile Forces”
or predators, parasites, diseases, food shortages, climate, and weather [see
Alexander 1977a] responsible for natural selection’s effects on gene frequencies)
by which variations in human social behavior and capacity are selected, by the
adjustment of strategies or styles of life, consciously and otherwise, by individu-
als and groups.
Few people would doubt that positive and negative reinforcement (learning)
schedules relate, respectively, to environmental phenomena reinforcing (1) sur-
vival and well-being and (2) avoidance of situations deleterious to survival and
well-being. With ordinary physical and biotic stimuli this relationship is easy to
understand: We withdraw from hot stoves, avoid poisonous snakes, seek out tasty
foods, appreciate warmth in winter, dislike getting wet in cold rains, etc. What
about social stimuli? Should it not be the same? Should we not seek social situa-
tions that reward us and avoid those that punish us? Should not the actual defini-
tions of reward and punishment in social behavior, as with responses to physical
stimuli, identify for any organism those situations that, respectively, improve or
insult its likelihood of social survival and well-being, with appropriate conno-
tations for reproductive success? Is it possible that Sheldon (1961) was right in
suggesting that “ . . . the reason why many pleasures are wicked is that they frus-
trate other pleasures”? That evil consists “in frustrations, as the Thomist says,
in privation of one good by another”? Is what is pleasurable, hence, “good” and
“right,” that which, at least in environments past, tended to maximize genetic
reproduction?

ARBITRARINESS IN CULTURE
The symbolic or seemingly arbitrary nature of many aspects and variants of culture
is commonly regarded as contrary to any functional theory, and especially to the
notion that culture can somehow be explained by a history of differential repro-
duction by individuals. Of course, seeming arbitrariness may represent observer
error based on failure to understand the significance of environmental varia-
tions. Arbitrariness may also be a consequence of the inertia to cultural change
in the face of environmental shifts; of mistakes about what kind of behavior will
best serve one’s interests—especially in the face of the constant and accelerating
introduction of novelty, primarily through technology. But, even if the assessment
of arbitrariness is actually correct, it need not be contrary to a theory based on
inclusive-fitness-maximizing, particularly if culture is explained as a product of
the different, as well as the common, goals of the individuals and subgroups of
individuals who have comprised human society during its history. Thus, however
symbolism and language arose- say, because they were superior methods of com-
munication—their existence, as the major sources of arbitrariness, also allowed
118 { Human Social Evolution

the adjustment of messages away from reality in the interests of the transmitting
individual or group. In other words, as abilities and tendencies to employ arbi-
trary or symbolic meanings increased the complexity and detail of messages, and
the possibility of accurate transmission under difficult circumstances (e.g., more
information per unit of time or information about objects or events removed in
time or space), they also increased opportunities for deception and misinforma-
tion. It would be a consequence that arbitrariness could typify some of the differ-
ent directions taken by cultural changes which were nevertheless crucial to their
initiators and perpetuators.
Consider the relationship between status and the appreciation of fashion, art,
literature, or music. What is important to the would-be critic or status-seeker is not
alliance with a particular form but with whatever form will ultimately be regarded
as most prestigious. If one is in a position to influence the decision he can, to one
degree or another, cause it to become arbitrary. Fashion designers, the great artists,
and the wealthy are continually using their status to cause such adjustments. In no
way, however, does such arbitrariness mean that the outcomes are trivial or unre-
lated to reproductive striving. Precisely the opposite is suggested that arbitrariness
may often be forced, in regard to important circumstances, because the different
circumstances involved represent important alternatives and because forcing arbi-
trariness is the only or best way for certain parties to prevail.
These various suggestions may simultaneously explain the genesis of “great
man” theories of culture and their failure as general explanations. Great men do
appear, and their striving, almost by definition, is likely now and then to have spe-
cial influences; but, for reasons given above, not necessarily great influences and
not influences leading to particular, predictable, overall changes in culture.
The old saw that “one hen-pecked husband in a village does not create a matri-
archy” also emphasizes not only that individuality of striving occurs within culture
but that it does not necessarily lead to trends. Similarly the argument about status
and arbitrariness is a variant of the adage that “when the king lisps everyone lisps,”
and it bears on the notion of a “trickle-down” effect in stratified or hierarchical
social systems. But it indicates that the “trickle-down” effect, rather than being
a societal “mechanism for maintaining the motivation to strive for success, and
hence for maintaining efficiency of performance in occupational roles in a system
in which differential success is possible for only a few.. .” (Fallers 1973) is a manifes-
tation of such striving, and a manifestation of degrees of success.
As already noted elsewhere in this volume, several recent studies have sug-
gested that many aspects of culture, involving such items as patterns of marriage,
inheritance, and kinship behavior, and varying in expression among societies, are
neither arbitrary nor independent of predictions from a theory dependent upon
inclusive-fitness-maximizing by individuals (Alexander 1977a).
Like learning theory and other theories that stop with proximate mechanisms,
Malinowski’s “functional” theory of culture, which was couched in terms of sat-
isfying immediate physiological needs, did not account for the existence of those
 Biology and Culture } 119

needs (Alexander 1977b). Thus, Sahlins (1976a) was led to say that for Malinowski
culture represented a “gigantic metaphorical extension of the digestive system.”
But Malinowski’s theory would have made sense in the terms suggested here if
it could only have been interpreted as seeing culture as a gigantic metaphorical
extension of the reproductive system.
The ideas I have just suggested are alternative to recent efforts to explain the
relationship of culture and genetic evolution—or, more particularly, their appar-
ent lack of relationship—by suggesting that “cultural instructions” (Cloak 1975) or
“memes” (Dawkins 1976) are selected in the same fashion as, and often in opposi-
tion to, genes or genetic instructions; or that two kinds of selection, often in oppo-
sition, are necessarily involved (Richerson and Boyd 1978). Arbitrariness, then, in
fashion or any other aspect of culture, may not be contrary to the genetic repro-
ductive success of those initiating and maintaining it, only to that of some of those
upon whom it is forced, in particular those who are least able to turn it to their
own advantage. To understand the reproductive significance of arbitrariness as a
part of status-seeking, one need only understand the reproductive significance of
status. One might suggest that there are genetic instructions which somehow result
in our engaging in arbitrariness in symbolic behavior in whatever environments it
is genetically reproductive to do so.
I’d suggest, then, that the rates and directions of mutability and heritability
in culture are determined by the collectives and compromises of interest of the
individuals striving at any particular time or place, together with the form and
degree of inertia in the cultural environment as a result of its history; that the “hos-
tile forces” that result in cultural change have tended increasingly to be the con-
flicts of interest among human individuals and subgroups in securing relief from
Darwin’s “Hostile Forces of Nature” (see above); and that, among these “Hostile
Forces of Nature,” increasingly prominent and eventually paramount have been
what amounted to predators, in the form of other humans acting in groups or in
isolation, with at least temporary commonality of interests (Alexander 1971, 1974,
1975a, 1977a).
By these arguments four outcomes are predicted: (1) a reasonably close cor-
respondence between the structure of culture and its usefulness to individuals in
inclusive-fitness-maximizing, (2) an even closer correlation between the overall
structure of culture and those traits which benefit everyone about equally, or
benefit the great majority, (3) extremely effective capabilities of individuals to
mold themselves to fit their cultural milieu, and (4) tendencies for culture to be
so constructed as to resist significant alteration by individuals and subgroups
in their own interests and contrary to those of others. If these predictions are
regarded as important we shall be led to analyze the variations in culture poten-
tially as the outcomes of different strategies of inclusive-fitness-maximizing
under different circumstances, and the proximate or immediate physiologi-
cal and social mechanisms whereby inclusive fitness is maximized as potential
explanations of degrees and directions by which cultural patterns diverge from
120 { Human Social Evolution

actual inclusive-fitness-maximizing behaviors when technological change and

other events create novel environments outside the limits of those in which ear-
lier behaviors functioned.

Concluding Remarks

I think we may regard as settled the universality and inevitability of natural selec-
tion and the rarity of effective selection above the individual level, and as relatively
trivial for social scientists the problem of the relative effectiveness of selection at
the individual level as against some lower level. I also suppose that culture can
evolve without genetic change, and that it does so frequently without diminution
of inclusive-fitness-maximizing effects. It would appear that the immediate future
in other areas of investigation will see concentration on two questions: (1) to what
extent are cultural patterns actually independent of predictions from natural selec-
tion, and why, and (2) how could patterns of cultural behavior be consistent with
natural selection in ways that do not do violence to our knowledge of the extent
and nature of learning? The papers in this volume suggest this trend and indicate
that in most cases the data, if they are to lead to convincing answers, will have to
be gathered with these questions actually in mind.
The complexity of the picture developed by these arguments and conclusions
indicates both the difficulty involved in extensive and thorough testing of an
inclusive-fitness-maximizing theory of human sociality and the potential gen-
erality of such a theory. Such testing is the major challenge that lies ahead on
the border between the social and biological sciences, together with the prob-
lem of dealing with the moral and ethical questions that arise along with any
increase in understanding of human behavior and how to modify it. The tasks
so identified are not likely to be easy or simple. But, then, no one who ever
thought about human behavior in analytical terms is likely to have supposed
that they would be.

References
Alexander, R. D. 1971. The search for an evolutionary philosophy of man. Proceedings of the
Royal Society of Victoria 84:99–120.
Alexander, R. D. 1974. The Evolution of Social Behavior. Annual Review of Ecology and
Systematics 5:325–383.
Alexander, R. D. 1975a. The search for a general theory of behavior. Behavioral Science
10:77–100.
Alexander, R. D. 1977a. Natural selection and the analysis of human sociality. In Changing
Scenes in the Natural Sciences, 1776–1976. C. E. Goulden, ed. Pp. 283–337. Academy of
Natural Sciences, Special Publication 12, Philadelphia: the Academy.
Alexander, R. D. 1977b. Evolution, human behavior and determinism. Proceedings of the
Biennial Meeting of the Philadelphia Science Association (1976). Vol. 2:3–21.
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Alexander, R. D. 1977c. Review of The Use and Abuse of Biology: An Anthropological

Critique of Sociobiology. American Anthropologist 79:917–920.
Alexander, R. D. 1978a. Natural selection and societal laws. In Science and the Foundation
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on-Hudson, New York: Hastings Institute of Society, Ethics and the Life Sciences.
Pp. 249–290.
Alexander, R. D. 1978b. Evolution, creation and biology teaching. American Biology Teacher
4(2):91–104.
Alexander, R. D. and Sherman, P. W. 1977. Local mate competition and parental investment
patterns in social insects. Science 196:495–500.
Alexander, R. D. 1979. Evolution, social behavior and ethics. In Science and the Foundations
of Ethics. IV. Hastings-on-Hudson, New York: Hastings Institute of Society, Ethics and
the Life Sciences.
Campbell, D. T. 1965. Variation and selection retention in sociocultural evolution. In
Social Change in Developing Areas: A Re-interpretation of Evolutionary Theory. H.
R. Barringer, G. L. Blankstern, and R. W. Mack, eds. Pp. 19–49. Cambridge, Mass.:
Schenkman.
Campbell, D. T. 1975. On the conflicts between biological and social evolution and between
psychology and moral tradition. American Psychologist 30:1103–1126.
Cloak, F. T. Jr. 1975. Is a cultural ethology possible? Human Ecology 3:161–182.
Darwin, C. 1967. On the Origin of Species. Boston, Harvard University Press (Facsimile of
the 1859 edition).
Dawkins, R. 1976. The Selfish Gene. Oxford: Oxford University Press.
Durham, W. H. 1976a. The adaptive significance of cultural behavior. Human Ecology
4(2):89–121.
Fallers, L. A. 1973. Inequality: Social Stratification Reconsidered. Chicago: University of
Chicago Press.
Ferguson, A. 1976. Can evolutionary theory predict? American Naturalist 110:1101–1104.
Hamilton, W. D. 1967. Extraordinary sex ratios. Science 156:477–488.
Harris, M. 1968. The Rise of Anthropological Theory. New York: T.Y. Crowell.
Hatch, E. J. 1973. Theories of Man and Culture. New York: Columbia University Press.
Mayr, E. 1963. Animal Species and Evolution. Cambridge, Harvard University Press.
Moore, J. N. and Slusher, H. S., eds. 1970. Biology: A Search for Order in Complexity. Grand
Rapids, Mich.: Zondervan Publishing House.
Murdock, G. P. 1960b. How culture changes. In Man, Culture and Society. H. L. Shapiro, ed.
Pp. 247–260. New York: Oxford University Press.
Peters, R. H. 1976. Tautology in evolution and ecology. American Naturalist 110:1–12.
Richerson, P. J. and Boyd, R. 1978. A dual inheritance model of the human evolutionary
process I: Basic postulates and a simple model. Journal of the Social Biological Structure
1:127–154.
Sahlins, M. D. 1976a. The Use and Abuse of Biology: an Anthropological Critique of
Sociobiology. Ann Arbor: University of Michigan Press.
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Sheldon, W.H. 1961. The criterion of the good and the right. In Experience, Existence and the
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111:386–390.
Trivers, R. L. and Willard, D. E. 1973. Natural selection of parental ability to vary the sex
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Williams, G. C. 1966. Adaptation and Natural Selection. Princeton, Princeton University
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6}

Intergroup Competition and Within-Group

Cooperation

THE OTHER SIDE OF THE SOCIAL COOPERATION COIN

A hydrogen bomb is an example of mankind’s enormous capacity for friendly

cooperation. Its construction requires an intricate network of human teams, all
working with single-minded devotion toward a common goal.
Let us pause and savor the glow of self-congratulation we deserve for belonging
to such an intelligent and sociable species.

— robert s. bigelow, 1969. The Dawn Warriors

Bragging Rights

Yesterday’s newspaper mentioned mass graves just discovered

where the other side was doing its thing not so long ago.
The next page bore a photograph of an old Afghan man,
arms outstretched, eyes imploring: eighteen, he said,
were sleeping together in his house,
all of his family, when our side dropped those bombs
aimed at enemies departed weeks before.
Two, the old man said, sobbing,
had emerged from the rubble,
two: he and his small daughter,
all that remained.
Today’s newspaper indicated that overall our side
is proud and happy because its bombs
have been 70% accurate.
Alexander, 2011, p. 20
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 Introduction

Thinking about Human Aggression, Past and Present:

Alexander and Tinkle’s (1968) Review of Lorenz and Ardrey
Bobbi S. Low

The altruistic tendencies of man most likely arose directly out of the interplay
between increasingly elaborate intergroup aggressiveness and intragroup
cooperativeness originating in parental behavior; the same process was more
than likely fundamental in the rapid evolutionary increase in man’s brain size.

—Alexander and Tinkle 1968: 2470

Writing (and reading) book reviews can be a real bore: the main types include the
“just the facts, ma’am” versions (“in chapter 3, evolution is covered . . . ”); the rant
by a dear enemy; the rave by an acolyte. But this is not your daughter’s book report;
written more than 40 years ago, this short piece foreshadows Alexander’s subtle
and encompassing theory of cooperation, and the interplay between cooperation
and aggression, as well as laying out, with remarkable sophistication for the time,
the interactions likely between natural selection—cultural selection—topics of
deep current interest.
Only two years after Williams’s 1966 Adaptation and Natural Selection,
Alexander and Tinkle made a clear argument for individual costs and benefits
driving cooperation, at a time when others (like my major professor) had not yet
thought through the difficulties in generating, maintaining, and spreading “spe-
cies adaptations” of the naïve group-selection sort. And they made the clear, novel,
argument that the driving force behind cooperation among males was not escap-
ing predators or finding food, but conspecific intergroup aggression; that is, that
other humans were (as they probably remain) the strongest selective forces in the
evolution of Homo. The force of conspecific arms races drove both aggression and
cooperation, and a rapidly enlarging brain (see “A New Theory of Cooperation”
introduced by Frank, this volume).
Alexander and Tinkle walked a fine line to delineate, as well as could be done
at the time, the fact that natural selection had surely shaped human aggression
and cooperation in context, despite a widespread then-current assumption that
126 { Human Social Evolution

there was no connection between any part of the human genotype and aggression.
Today we know about some genetic influences (as is usual, from uncovering cases
that are so far from normal as to be noticeable); but Alexander and Tinkle were
effective long before this knowledge, by pointing out that costs and benefits of
aggression and cooperativeness differed for various individuals with the context,
and that open aggression was more often profitable for males rather than females.
So, before the term “behavioral ecology” really existed, Alexander and Tinkle
laid out the argument that the particular structure of human groups (in time,
space, composition), combined with sociality and intelligence, led to the develop-
ment of a delicate and complex within-group balance between cooperation and
competition, and increasingly intense between-group competition. Alexander
continued to develop theoretical aspects of the intelligence-cooperation-compe-
tition tension (e.g., 1979, 1986, 1987), and Flinn and colleagues (2005) have fleshed
out Alexander’s argument further.
Alexander was amazingly prescient; even today there are papers asking whether
human group structure might influence behavioral ecology (e.g., Bowles 2009)—
yet Alexander and Tinkle raised this issue more than 40 years ago, and set it in the
broadest (and most relevant) context: that of reproductively important resources.
Others followed (Chagnon 1997; Wrangham 1985; Manson and Wrangham 1991;
Low 1993, 2000; ch. 13, this volume) but we were merely filling in the details. The
main outlines of the argument were set out in this short piece. In traditional soci-
eties, a man’s skill in war tended to be closely tied to his lifetime reproductive
success. As a Yanomamö man made clear to Napoleon Chagnon (1997: 191) in dis-
cussing raids, it is really all about women and the resources to get them, whether
those are cattle, sheep, goats, or something else.
Perhaps the historical oddity of a grand-scale Cold War in the twentieth cen-
tury obscured the importance of individual and coalitional striving—striving that
evolved because it influenced reproductive success. That is the core; in proximate
terms, one can list endless “causes” of warring. Even scholars of military history
tended to miss the importance of intergroup conflict as reproductive strategy,
though the historian John Hale (1985:22) called warfare through the Middle Ages
“violent housekeeping,” which does suggest individual offense and defense focused
on resources. From very small tribal conflicts on, leaders and skillful fighters tra-
ditionally fought in the middle of the fray; since the Middle ages, as John Keegan
(1987) noted, commanders have moved farther from danger and the “front” so
that risks and benefits to fighting grew ever more separate. But the functional sig-
nificance of the evolution of coalitions to fight other groups’ coalitions has not
changed.
Not every observation Alexander and Tinkle made turns out to be strictly true,
but their argument is solid. They named humans as the only group other than
social insects that made war; we know now that, for example, vervet monkeys
have intergroup aggression over range boundaries (Cheney 1986); and chimpan-
zee males go on raids much like the Yanomamö (e.g., Manson and Wrangham
 Intergroup Competition and Within-Group Cooperation } 127

1991, Mitani et al. 2010, Watts et al. 2006), though neither of these cases is entirely
comparable (nor are ants). Human warfare may, however, be unique among intra-
specific intergroup conflict, in having “disinterested” third-party involvement
(e.g., within-nation legal powers, United Nations peacekeeping forces), as well as
having a separation across individuals in who pays the costs and who reaps the
benefits of warfare, from “taking the King’s shilling” to the US draft, and today’s
US recruitment primarily of young men who have few other prospects. It is true
that the institutions don’t always work, as in the Rwandan genocide, but they are
unique in existing at all. (This is another phenomenon on which Alexander later
expanded: e.g., Alexander 1986, 1987.)
Alexander and Tinkle suggested that small group size may have mandated some
rather close inbreeding, resulting in the favoring of intensive outbreeding in some
groups. Perhaps, but first-cousin marriages (prohibited in 25 US states, allowed in
another six only if the individuals cannot reproduce, or in one case [Maine], have
a certificate of genetic counseling) are in fact, preferred marriage forms across
traditional societies. The commonest types of cousin marriage across traditional
societies reinforce the general argument Alexander and Tinkle make (and which
Alexander expanded explicitly in 1979: 15): Most of these societies are patrilocal,
and “father’s brother’s daughter” is the associated preference. Avunculocal and
matrilocal residences favor other arrangements (father’s sister’s daughter, and
mother’s brother’s daughter). Both resources and male-male cooperation within
group are at stake (e.g., Flinn and Low 1986). Interestingly, the one type that would
round out our survey—mother’s sister’s daughter—is virtually unknown, probably
because women in most traditional societies control few resources, and do not, as
do vervet monkey females, fight openly in intergroup conflicts.
So even particular “not-quite-facts” of their time, when we find out more, con-
tribute to Alexander and Tinkle’s general argument. For me, the saddest statement
that turned out not to be true was: It is a significant step forward that the questions
receiving attention today are not whether man evolved, but how he evolved. I think
that statement was made more in hope than conviction. During the late 1960s and
the 1970s, Alexander publicly debated noted creationists, hoping, perhaps, to make
that statement come true. Nonetheless, today we have thinly disguised creationism
in the “intelligent design” group, and 44% of Americans are sure that humans did
not evolve, but were created (presumably with all other life forms) by God in the
last 10,000 years (Dawkins 2009, citing a 2008 Gallup poll). If you include those
who think humans did evolve, but under God’s guidance, the total is 80%.
One aspect peculiar to Dick was that whenever he wrote anything, he ended
up trying to explain the world. In longer pieces, this could be frustrating. (Once,
when I was working on historical demography, I thought I remembered that he
had made a prescient comment in print about demographics. I asked him, and
he said yes, he had—but he couldn’t remember where, and I never did find it
again.) But in short reviews, this tendency has a mind-expanding impact; tak-
ing on human evolution, the interplay between aggression and cooperation, gets
128 { Human Social Evolution

readers thinking about more than what Lorenz and Ardrey had written, and that is
crucially important. In another review on a book on biological control, Alexander
(1975) raised, far before others were thinking about it, what is now called the “pes-
ticide treadmill” and the evolutionary problem of how, by relying on pesticides
and herbicides in agriculture, we simply select for ever-more-resistant pests, a
problem that still plagues us today.
Alexander and Tinkle ended with a crucial caveat worth remembering:
Finally, we do not believe, as Ardrey and Lorenz both imply, that knowledge
concerning man’s evolutionary history, regardless of the revelations it may
involve, can in any way restrict what man is able to accomplish in manipu-
lating his own behavior toward any desired end. Knowledge of our evolu-
tionary background cannot close doors; it can only open them.
May it be so.

References
Alexander, R.D. 1975. Natural enemies in place of poisons. Nat. Hist. 84(1): 92–95. (Book
review of Paul DeBach’s Biological Control by Natural Enemies.)
Alexander, R.D. 1979. Darwinism and Human Affairs. Seattle: University of Washington
Press.
Alexander, R.D. 1986. Biology and law. Ethol. Sociobiol. 7: 167–173.
Alexander, R. D. 1987. The Biology of Moral Systems. Hawthorne, NY: Aldine DeGruyter.
Bowles, S. 2009. Did warfare among ancestral hunter-gatherers affect the evolution of
human social behaviours? Science 324:1293–1298.
Chagnon, N. 1997. Yanomamö. 5th ed. Ft. Worth, TX: Harcourt Brace.
Cheney, D. 1986. Interactions and relationships between groups. In: B. Smuts, D, Cheney,
R. Seyfarth, R. Wrangham, and T. Struhsaker (eds.), Primate Societies. Chicago:
University of Chicago Press, pp 267–281.
Dawkins, R. 2009. The Greatest Show on Earth: The Evidence for Evolution. New York: Free
Press.
Flinn, M., Geary, D., and Ward, C. 2005. Ecological dominance, social competition, and
coalitionary arms races: Why humans evolved extraordinary intelligence. Evol. Hum.
Behav. 26: 10–46.
Flinn, M., and Low, B. 1986. Resource distribution, social competition, and mating pat-
terns in human societies. In: D. I. Rubenstein and R. W. Wrangham (eds.), Ecological
Aspects of Social Evolution: Birds and Mammals. Princeton, NJ: Princeton University
Press, pp. 217–243.
Hale, J.R. 1985.War and Society in Renaissance Europe. New York: St. Martin’s Press.
Keegan, J. 1987. The Mask of Command. London: Jonathan Cape.
Low, B. 1993. An evolutionary perspective on war. In: H. Jacobson and W. Zimmerman
(eds.), Behavior, Culture, and Conflict in World Politics. Ann Arbor: University of
Michigan Press, pp. 13–56.
Low, B. 2000. Why Sex Matters. Princeton, NJ: Princeton University Press.
 Intergroup Competition and Within-Group Cooperation } 129

Manson, J., and Wrangham,V. 1991. Intergroup aggression in chimpanzees and humans.
Curr. Anthro. 32(4):369–390.
Mitani, J., Watts, D.P., and Amsler, S.J. 2010. Lethal intergroup aggression leads to territorial
expansion in wild chimpanzees. Curr. Biol. 20(12): R507–R508.
Watts, D., Muller, M., Amsler, S., Mbabazi, G., and Mitani, J.C. 2006. Lethal intergroup
aggression by chimpanzees in the Kibale National Park, Uganda. Am. J. Primatol. 68:
161–180.
Williams, G.C. 1966. Adaptation and Natural Selection. Princeton, NJ: Princeton University
Press.
Wrangham, R. 1985. War in evolutionary perspective. In: D. Pines (ed.) Emerging Synthesis
in Science. Santa Fe, NM: Santa Fe Institute, pp. 123–132.
 A COMPARATIVE REVIEW

Excerpt from Alexander, R.D., and Tinkle, D.W. 1968. Review of On Aggression
by Konrad Lorenz and The Territorial Imperative by Robert Ardrey. Bioscience
18:245–248.

On Aggression, by Konrad Lorenz, Harcourt, Brace & World, New York, 1966.
The Territorial Imperative, by Robert Ardrey, Atheneum, New York, 1966.

Few recent books have been reviewed as many times in rapid succession, or with
as much vehemence in both defense and derogation, as On Aggression by Konrad
Lorenz (1966, Harcourt, Brace and World) and The Territorial Imperative by
Robert Ardrey (1966, Atheneum). The principal reason for this attention—and for
the disagreements—is that Lorenz and Ardrey have tried to write about one of the
most sensitive and important questions facing man: his nature as determined by
and determinable from his evolutionary history. The two books have often been
reviewed together because they share the basic theme that man is an aggressive
animal and that this aggressiveness is in some way a product of the evolutionary
process. On Aggression is a personal commentary from a professional zoologist
with an extensive background of training, thought, and investigation in behavioral
biology. Ardrey, on the other hand, is no biologist, but he has produced a fascinat-
ing narrative that is remarkably well-documented. Unfortunately, one of its fasci-
nating aspects is the disarming ease with which it travels back and forth between
major insights and ridiculous oversimplifications. Both men write in ways tending
to rekindle old, pointless arguments of the instinct vs. learning variety. Although
they profess to be presenting evolutionary arguments, both men have mixed into
their discussions some peculiarly nonevolutionary or antievolutionary themes.
Man is indeed an elaborately aggressive organism, and the nature of the evo-
lutionary background for this aggressiveness is a legitimate problem. He is also
probably the most extensively altruistic of all organisms. Ardrey and Lorenz take
the evolutionary basis of his aggressive tendencies as their major themes, but, in
general, seem to muddle the problem of evolving his altruistic tendencies. Critics
argue that the prominence of these seemingly opposed tendencies in man’s behav-
ior indicates that the characteristic that really evolved was merely the capacity
for either behavior, as the situation demanded. They contend that the develop-
mental basis of such behaviors in man is too complex, and that they are too indi-
rectly related to the genotype, for selection to accumulate genes directly correlated
with either aggression or altruism as such. We believe that this view, too, is an
 Intergroup Competition and Within-Group Cooperation } 131

oversimplification. It would be naive to try to explain man’s preoccupation with

sex without reference to natural selection; perhaps it is only a little less naive to do
so with aggression.
The nature of the evidence on which reasonable answers about man’s evolution-
ary history can be based and the problem of what it means for man to make dis-
coveries about himself regarding such attributes as aggression and altruism are the
important questions that arise from reading Lorenz’s and Ardrey’s books. Several
previous reviewers have concentrated on detailed criticisms; we would like instead
to consider the general question of the role of aggressiveness and territoriality in
man’s evolution and build an hypothesis on what we think are appropriate atti-
tudes toward these human attributes. We will also try to identify what we believe
are flaws in Lorenz’s and Ardrey’s arguments.
It is a significant step forward that the questions receiving attention today are
not whether man evolved but how he evolved. Doubt seems no longer to exist
in the minds of reasonable and knowledgeable persons that man is a product of
evolution—a result of the same basic process that has produced all life. A major
consequence of this realization is that whatever characteristics may be construed
to be uniquely or most decidedly human are thereby automatically categorized as
producible through natural selection.
If the size of his brain is used as the chief index to man’s evolutionary divergence
(and this seems reasonable not only because of the importance of brain function in
specifying man but also because brain size increases correlate with paleontologi-
cal and archeological evidence of increasing complexity of social organization and
various cultural phenomena), then there seem to be at least three major puzzles
concerning man’s evolution from a nonhuman primate:

1) How could his brain increase in size so rapidly from australopithecine

to modern man (50–150,000 generations)?
2) What caused the increase in brain size to go so far beyond that of all
other primates?
3) What caused the brain apparently to stop increasing in size some
50–100,000 years ago?

Regardless of the indirectness of the relationship between man’s genotype and

those aspects of his phenotype that we generally refer to as “intellect,” we must
conclude that variations in intellect were subjected to unusually intense selective
action, that this selection was consistent across a long period, and that it carried
man’s intellectual capabilities right up to their present condition.
Let us consider the basic process by which natural selection operates. First, it
always involves competition between alternate genetic elements within species.
Even in interspecific competition, evolution occurs as a result of some variants
within one or both species outreproducing the other variants. Although selection
actually works through favoring certain individual organisms, the result is change
in gene frequencies in populations.
132 { Human Social Evolution

There seem to be three possible kinds of intraspecific competition or three

different levels of intensity at which selection can operate on alternative genetic
elements:

1) Differential reproduction without direct interaction, and no

confrontation between competitors.
2) Partial or complete exclusion of competitors from the best (or only)
sources of food, mates, and shelter through aggressiveness and
territoriality.
3) Elimination of competitors or potential competitors by killing them;
this could include cannibalism, or the elimination of competitors with
food being obtained without additional risk or energy expenditures.
Of these kinds of intraspecific competition, the first would usually result in the
slowest evolutionary change, the others, in order, in increasingly rapid change. The
questions we would ask about man’s evolution are (1) which kinds of competition
were involved, (2) which were most likely predominant, and (3) what were the
sizes and compositions of the units among which each kind of competition oper-
ated? In other words, which operated only among individuals and which among
social groups, such as families, of different sizes and complexities?
Differential reproduction without direct competition occurs in every species
of organism, whether or not the other forms of competition also occur. Exclusion
of competitors through aggression or some form of territoriality is widespread
among animals with complex behavior - such as vertebrates, arthropods, and
cephalopods and may be universal among such organisms during times when
food, shelter, or mates are in short supply. Nearly all modern primates seem to be
territorial.
Killing of competitors and cannibalism are rarely observed, and it is usually
difficult to obtain evidence whether observed cases represent evolved functions
or incidental effects resulting from some other kind of selective action. Few ani-
mals seem to be cannibalistic—none as much as man’s fossil record suggests was
the case during his evolution. On the other hand, reviewers of these books who
emphasize that little intraspecific violence occurs in most animals in the wild are
simply reminding us that responses to aggression also evolve. That ritualization
and threat can be effective in establishing dominance without injuries or death
is only evidence that inhibition of aggression as well as aggression is subject to
natural selection. Aggressive interactions are also crucial when they are conducted
solely by threats; such ritualization, on the other hand, is only effective when, on
the average, the subordinate gains by giving in. When commodities (food, shelter,
mates) are in sufficiently short supply, no advantage is to be gained by giving up.
Unlike Lorenz and many other behavioral biologists, we do not find it reasonable
or necessary to consider either inhibition of aggression or altruistic behavior as
“species” adaptations, evolved to assist the species at the expense of the reproduc-
tion of the individuals showing such responses.
 Intergroup Competition and Within-Group Cooperation } 133

The chances seem remote that man evolved without a significant amount of
intraspecific aggression occurring continuously and, in fact, guiding his evolution
to some extent. We would go further and agree with Lorenz and Ardrey that a
more elaborate and extensive array of intraspecific aggressiveness may have been
involved in man’s evolution than in that of any other animal. This is not to say
that any particular kind or instance of human aggression at present may not have
grown out of a purely cultural context. We are simply agreeing that, during a long
period—perhaps all—of man’s evolution, aggressive behavior was directly favored
by selection. Under these circumstances there must have been increases in the
frequency of many genes that increased the effectiveness of aggression. As with
most other human traits, and all human behavior, it is difficult to understand the
developmental and hereditary basis of aggressive behavior in any individual or any
particular instance; selective action on such a trait must operate in exceedingly
indirect fashions. Aggressiveness may easily be modified by culture, and discern-
ible variations in aggressiveness based on genetic differences may be rare or absent
among men today. These facts, however, cannot be used to deny the possibility of
a genetic background for either the general intensity and quality or the prevalence
of aggressiveness in humans. Neither do such conclusions lead us to the remark-
able parallels Ardrey draws when he supposes, for example, that a scientist who
“place[s] at the disposal of the machinery of war the most sophisticated attain-
ments of his discipline” is “fill[ing] out from the particularity of his learning the
generality of that open instinct, the territorial imperative, and, having done so ...
[acting] according to the finished pattern with the predictability of a capricorn
beetle.”
Excluding certain social insects, man is the only warring species, and one of the
few that commonly engages in interindividual death battles. Perhaps only in man
are all of the necessary abilities for such behavior combined. Other animals never
developed necessary equipment for killing conspecifics, lack ability to organize
for group warfare, lack the ability for recognizing and sparing near relatives, or
have been unable simultaneously to resolve the conflicting necessities of intra-
group (or family) tolerance and intergroup hostility. In any species engaging in
the more violent kinds of intraspecific competition, ability to recognize and spare
close relatives would be highly favored. Such an effect, moreover, would have been
facilitated by man’s tendency to live in small bands or family groups. Members of
one’s own band could automatically be treated as relatives, or tolerated and even
assisted; those of other bands could equally automatically be treated as competi-
tors or the enemy.
Let us take a closer look at what early man was presumably like in order to
understand better the significance of the above suggestions. Sometime during
his early evolution man became more carnivorous than any modern primate. He
hunted his food, and this would have placed a selective premium on individuals
capable of improving their weapons, their bipedal locomotion, and their ability to
hurl weapons at elusive prey.
134 { Human Social Evolution

Up to this point, there may have been relatively mild selection favoring larger
brains (by which is implied—properly, we believe—more complex brain function).
Cooperation among individuals of a family in hunting could have favored effec-
tive communication systems which would have, in turn, allowed for passing on
more cultural information to offspring. Such families, with the favorable genetic
endowment of larger brains and thus better ability to absorb and remember past
experiences and to associate cause and effect relationships, must have been bet-
ter hunters and also better at transmitting to offspring the benefits of experience.
There must also have been sexual selection in the same contexts, for it would cer-
tainly have been to the advantage of females to choose among potential mates
those whose intelligence and hunting prowess would cause the maximum survi-
vorship of their offspring.
One way or another, family groups evidently increased in size, consisting of
more than a pair of adults, and perhaps in some cases three generations of indi-
viduals, all of which had more in common, both genetically and culturally, than
they had with members of other such groups. The degree of inbreeding may have
been rather high within such groups. This could have resulted in the rapid fixation
of certain genotypes and favored intensive outbreeding within groups, owing to
prevalence of genes deleterious in the homozygous condition, perhaps leaving an
effect in incest taboos of modern man.
As males in family groups aged, they would be unable to maintain dominant
positions. However, it may have been of advantage to younger members of the
group to tolerate such individuals, thereby benefiting from their experience and
wisdom. Such behavior would not only select for long adult life but make for greater
cohesiveness between generations and cause groups to increase in size without
fragmentation and to persist longer. Cooperation between parents and grandpar-
ents might allow surer recognition and encouragement of offspring in culturally
transmissible skills such as tool making and hunting. It could free younger adults
for hunting and other essential activities, and it would allow a longer period for
passing on the accumulated culture to each successive generation. Such processes
as these should rapidly incorporate into a stable and long-persisting group not
only genes for greater intelligence but also any useful cultural attributes intro-
duced into the group. Under such conditions, “postreproductive” becomes a dif-
ficult term to define.
The social structure of early man was also probably conducive to the develop-
ment of elaborate intraspecific aggression. Each family group would have differed
from every other one in cultural as well as genetic traits, to a degree depending
upon its stability and cohesiveness. The individuals of such groups were surely
able to recognize members of their own group, and, further, to recognize some of
their closer relatives (at least their own offspring) within the group. Direct aggres-
sion between family groups could have resulted in rapid shifts in gene frequencies
in the population as a whole. On the other hand, altruistic behavior toward other
individuals within groups would also have been favored by selection, both because
 Intergroup Competition and Within-Group Cooperation } 135

of the necessity of belonging to a group and because it would result in the favoring
of genetically related individuals. Intragroup cooperativeness does not preclude
intragroup competition, as, for example, in baboon colonies today.
Elaborate parental behavior, which includes both recognition of relatives and a
kind of altruism (toward one’s offspring), and elaborate aggressive and territorial
behavior go hand-in-hand in a wide array of animals. They are almost universally
linked. It seems to us that man’s altruistic tendencies, as well as his aggressiveness,
could have been favored by ordinary natural selection. There is no need to involve
the supernatural or to speak of “species” adaptations. We do not understand
Ardrey’s tendency to divorce aggressive and reproductive behavior; aggressive and
territorial behavior cannot evolve unless it enhances reproduction, and there is
no evidence making this argument problematic in any way. We certainly disagree
with Lorenz’s conclusions that man failed to develop inhibitions to aggression and
that this was because for a long period of his history he was unable to kill his
fellow man.
Let us consider in more detail the extent and nature of intergroup aggression in
early man. As a result of spatial isolation of family groups and an exclusive kind of
social organization such as occurs in many primates (and man) today, each family
group would have been to a large extent a gene pool and micro-culture of its own.
Different groups might be expected to have varied in average intelligence, in the
degree of intragroup cooperation, and in the nature of weapons, hunting ability,
and experience.
If shortages of essential commodities such as food and shelter were the rule,
then when groups contacted one another, we suppose that one usually attacked the
other, killing the males and possibly the young, and appropriating the females. The
successful band in these battles could accumulate experiences increasing the prob-
ability of success in subsequent encounters. Repetition of intergroup interactions
should select for greater intelligence, increasing aggressiveness between groups,
and, simultaneously, increasing cooperativeness and altruism within each group.
In short, we visualize a situation in man’s early hunting ancestry in which repro-
ductive individuals characteristically lived in groups, and in which some groups,
possessing higher frequency of individuals of greater intelligence, were able by
intragroup cooperation and communication to exterminate and replace adjacent
groups. Such a process could bring about increasing uniformity among surviv-
ing groups, by assimilating intergroup genetic and cultural variation faster than
it could be produced, and ultimately decrease the profit to be gained from direct
intergroup strife. As this condition was approached, more cohesiveness among
splintering bands might have led to sizeable tribes and nations with a correspond-
ing extension of the allegiances of individuals.
What forces could have promoted cohesiveness in band structure? Large preda-
tors eliminate lone individuals or small groups among modern primates that live in
tightly organized bands. This may be the only kind of selective action that has pro-
duced large bands in primates. Intraband competition, promoted by recognition
136 { Human Social Evolution

of near relatives deriving from complex parental activities, would run counter to
increases in band size and cohesiveness. Advantages deriving from cooperation
in killing large game have often been used to explain development of large bands
of primitive men. This not only presumes a dependence upon large game, but it
does not seem likely to explain groups of more than a dozen or so able-bodied
hunters. Furthermore, as man’s weaponry improved and his behavioral complex-
ity increased, the minimal size of groups effective in this context would decrease,
not increase.
For long periods during man’s evolution organized bands may have served as
protection against, not other species of predators, but other bands of humans. In
such case there would be no theoretical upper limit on band size. If intraband
selection worked continually against increasing band size and cohesiveness, then
we would expect that reduction of interband friction resulting from lowered pop-
ulation density (for example, from disease), tendencies toward agriculture, and,
eventually, the development of means of protecting large groups within which
each family had its own territory (armies and farms) would result in shifts toward
increased isolation of small family groups and coincidentally toward monogamy.
To return now to the three questions given at the outset, we believe that man’s
brain size increased so rapidly and diverged so far from the brains of other pri-
mates (1) because man’s chief competitors all during his evolution were other men
and (2) because the competition was of a most direct and extensively aggressive
sort, an increasing amount of it operating between family groups of growing size
and complexity and with increasingly effective cultural transmission. We believe
that brain size stopped increasing when culture became so elaborate and social
groupings so large and complex that recognition of allies largely lost its associa-
tion with degree of genetic relatedness. The result would have been a re-direction
of altruistic behavior previously directed toward genetic relatives until its selective
advantages were reduced or nullified. As a result, genetic variations reflected in
variations in brain size or complexity would largely lose their selective advantage,
and evolutionary increases in brain size would level off.
From the preceding discussion, several useful questions arise for the con-
tinued investigation of man’s evolutionary history: What was the breeding and
social structure of known groups of early man and how much group interchange
occurred? How were new bands formed? What was the extent of intergroup
aggression? How was intragroup competition expressed? When did cultural
means of recognition of fellow band members or tribesmen arise? Were males
and young and old members of competing groups ordinarily killed by victorious
bands? Were males more often eaten in cannibalistic ceremonies? Was the degree
of cooperation between bands a function of the degree of their genealogical rela-
tionship? Not all of these questions can be answered in regard to primitive man,
but they provide a frame of reference. They are the same questions that should
be asked, but often are not, with regard to the behavior of other primates and so-
called primitive men still in existence today.
 Intergroup Competition and Within-Group Cooperation } 137

To conclude, the story of man’s evolution seems to have been that of individu-
als becoming able to recognize themselves as members of larger and larger groups
of increasing complexity of social organization. The altruistic tendencies of man
most likely arose directly out of the interplay between increasingly elaborate
intergroup aggressiveness and intragroup cooperativeness originating in parental
behavior; the same process was more than likely fundamental in the rapid evolu-
tionary increase in man’s brain size. Man’s tendency to become involved in wars
was almost surely directly favored by selection for a long period of his evolution
and, therefore, in some important sense, is not a kind of degenerate or degraded
behavior resulting from civilization.
Finally, we do not believe, as Ardrey and Lorenz both imply, that knowledge
concerning man’s evolutionary history, regardless of the revelations it may involve,
can in any way restrict what man is able to accomplish in manipulating his own
behavior toward any desired end. Knowledge of our evolutionary background
cannot close doors; it can only open them. If man’s history did involve “nature red
in tooth and claw,” it is no less to our advantage to comprehend where we have
been, and possibly of very great benefit in insuring that we realize whither it may
be that we wish to go and the best way of moving in that direction.
Richard D. Alexander and Donald W. Tinkle
Museum of Zoology and Department of Zoology
University of Michigan, Ann Arbor
7

Kinship, Parental Care, and Human Societies

To a Life Mate
should we be primitives you and I
could lie together naked between bearskins
staring at the night-time sky
listening to the forest
and dreaming sweet sadnesses
about all that must have gone before us
and all that must come after
Alexander 2011, p. vii
 INTRODUCTION

Concealed Ovulation in Humans: Further Evidence

Beverly I. Strassmann

Introduction to Alexander, R.D. and Noonan, K.M. 1979. Concealment of

Ovulation, parental care, and human social evolution. In N.A. Chagnon and
W.G. Irons (eds.). Evolutionary Biology and Human Social Behavior: An
Anthropological Perspective. 436-453. North Scituate, MA: Duxbury Press.
I first met Richard Alexander in 1976 when he directed my summer efforts to
help my sister Joan with her research on paper wasps (Polistes annularis). This
study entailed standing on a ladder painting dots on the wasps, sticking it out as
long as possible while the wasps grew increasingly agitated. In the Texas heat, my
sister wisely wore a bee veil and painter’s coveralls while I wore skimpier clothing
and got lots of wasp stings. At the end of the summer, I met with Alexander in
his office in the Museum of Zoology and he asked me: “What is kin selection?”
Alexander was unique among professors in his enthusiasm for discussing sci-
ence one-on-one with undergraduates and his wonderful courses (Evolution and
Human Behavior and Evolutionary Ecology) were in a league of their own. His
legacy includes the many evolutionary biologists and anthropologists who got
their scientific start in these courses.
I was fortunate that during my undergraduate years Alexander was writing
Darwinism and Human Affairs (D&HA)—the book that developed his theoretical
insights about evolution and culture, as well as nepotism and reciprocity. I feel that
I was witness to an important time in the history of science. More than 30 years
later, D&HA is still being translated into additional languages. During my first
year (1986–1987) of Ph.D. fieldwork among the Dogon of Mali, I used D&HA to
teach evolutionary theory to my research assistant, Sylvie Moulin. We had a small
house in a remote village with a shade shelter next to an ancient baobab. Sylvie
would read D&HA amid the cacophony of weaver finches and ask me questions
about difficult paragraphs. In this African field setting where most human interac-
tions take place in a web of kinship, D&HA came dramatically to life. Sylvie aban-
doned her competing reading material, Clifford Geertz’s Understanding Culture, to
the cobwebs in a corner of her room.
Alexander sparked fire in the minds of his undergraduate students by giving
them the opportunity to figure out answers to problems in biology that hadn’t
already been fully solved. We were expected to come up with something original,
140 { Human Social Evolution

and he challenged us to write a publishable essay—possibly one that would iden-

tify an error he had made. I wrote my essay, “Sexual selection, paternal care, and
concealed ovulation in humans,” on an idea that sprang from Alexander’s article
with Katie Noonan (1979). They began their article with a discussion of distinc-
tively human attributes—attributes not expressed in other species to the degree
that they are in humans, including consciousness, foresight, tool use, language,
and culture. To this list they added 25 additional traits, many of which are “sexu-
ally asymmetrical,” reflecting in particular “interactions of the sexes in connection
with parental care.” The crux of their argument is that as intergroup competition
became a principal guiding force in human evolution, the complexity of social
competition and cooperation within groups increased, selecting for intelligence,
consciousness, and foresight, as well as for increased parental care to impart social
skills to offspring.
Intergroup competition had not previously been invoked to explain either the
distinguishing human attributes or the unusual extent and duration of paren-
tal care in humans relative to other primates. Looking back, it is clear that the
Alexander and Noonan article was a scientific watershed because it stimulated
a vast literature and has stood the test of time. For example, Bowles and Gintis
(2011) recently emphasized intergroup competition as the driving force for intra-
group cooperation in humans and their arguments trace directly back to Richard
Alexander.
Testing the hypothesis that paternal care is crucial for offspring survival
and social success is currently an active area of research in human behavioral
ecology. Strongly supportive evidence for the hypothesis has been found in the
Ache of Paraguay where children without fathers were 3.9 times more likely
to be killed in each year of childhood and children of divorced parents were
2.8 times more likely to be killed (Hill and Hurtado 1996). Many studies in
other societies found no association between paternal presence and juvenile
survival—perhaps because mothers, grandparents, and other individuals took
up the slack when the father was absent (see Winking et al. 2011). Although
fathers in many societies engage in little direct care of infants, they have an
important effect on the social competitiveness of offspring—the paternal
role emphasized by Alexander and Noonan. Among the Martu aborigines of
Australia, for example, the presence of fathers is associated with an earlier
age at initiation, which is the gateway to reproduction for sons (Scelza 2010).
Comparative data on humans and other primates link the evolution of paternal
care to the development of pair bonds, as suggested by Alexander and Noonan’s
scenario for the evolution of concealed ovulation (Fernandez-Duque et al.
2009). Recent research on neuroendocrine mechanisms has shown that lower
testosterone and higher prolactin levels are markers of fatherhood and pair-
bonding (Gray et al. 2002, Gray et al. 2007, Alvergne et al. 2009). Paternal care
is not merely a cultural overlay; instead it is supported by a suite of evolved
proximate mechanisms.
 Kinship, Parental Care, and Human Societies } 141

CONCEALED OVULATION
Alexander and Noonan’s pivotal contribution was to link increased paternal
investment in humans to paternity certainty and the evolution of concealed
ovulation. They argued that the advertisement of ovulation might cost a
female her mate’s parental investment in two ways: “(1) by attracting compet-
ing males who threaten his confidence of paternity, and (2) by freeing him,
after a brief consort period, to seek copulations with other fertile females who
would compete later with her for his parental care” (Alexander and Noonan
1979, p. 443). In my paper for Alexander’s course, I added a further argument
that stemmed from the tradeoff between mating effort and parental effort in
males (Strassmann 1981). I suggested that subordinate males who are the least
successful at getting multiple mates would have the most to gain by paternal
behavior, while the males successful as polygynists would gain least. Further,
I suggested that the concealment of ovulation was favored by selection because
it enabled females to garner the paternal investment of subordinate males with
whom they had a confluence of interest. Both subordinate males and females
benefited from increased paternal investment (Strassmann 1981). Alexander
and Noonan had suggested that the dominant males would be the first to enter
into pair bonds with females concealing ovulation. In primate species, domi-
nance rank and reproductive success are usually correlated, but the evidence
has supported the view that females sometimes prefer middle or low-ranking
males (Wroblewski et al. 2009).
In his 1990 paper “How did humans evolve?,” Alexander used strong logical
arguments to reject the other hypotheses (Symons 1979, Benshoof and Thornhill
1979, Burley 1979, Hrdy 1979) that appeared the same year (1979) that he and
Katherine Noonan published their article. His discussion of these hypotheses (ch.
7, this volume) illustrates the technique of strong inference (Platt 1964) and shows
Alexander’s uncanny ability to test alternative hypotheses using qualitative infor-
mation. His 1990 paper explains why females evolved to conceal ovulation not
only from their mates but also from themselves. Females who were conscious of
their own ovulation would be in an excellent position to obtain good genes outside
the pair bond but would assume the risk associated with continually deceiving an
“intimate associate” about the timing of ovulation. Moreover, if females exploited
their knowledge of the timing of ovulation, then selection would favor males who
withheld paternal investment. Female deceit, in conjunction with continued male
paternal investment, would not be evolutionarily stable.

RECENT CLAIMS FOR “HUMAN OESTRUS” AND “OVULATORY CUES”

Alexander and Noonan’s hypothesis on concealed ovulation has been scruti-

nized by countless biologists, anthropologists, and evolutionary psychologists.
One recent argument is that ovulation in women is not concealed after all (e.g.,
Haselton and Gildersleeve 2011, Gangestad and Thornhill 2008). This reaction is
142 { Human Social Evolution

due to a misperception that ovulation is concealed only if there is a total absence

of detectable phenotypic changes during ovulation. Instead, what Alexander and
Noonan (p. 442) actually sought to explain were the reasons why natural selection
reduced the conspicuousness of ovulation in the human lineage:

In nonhuman primates the general period of ovulation always appears to

be more or less dramatically signaled to males (even if only by pheromones
or other means not obvious to human observers). All of the nonhuman pri-
mates in which females are known to show “pseudo-estrus” are group-living
species, while the least obvious signs of ovulation seem to occur in monoga-
mous species like gibbons, or polygynous species, like gorillas, which tend
to live in single-male bands. Human females are thus unique in that they give
little or no evidence of ovulation and may be receptive during any part of the
ovulatory cycle. Although some women have discovered ways to determine the
time of their ovulation, it is clear that selection has reduced the obviousness of
ovulation during human evolution, apparently to women themselves as well as
to others (emphasis added).

The hypothesis that human females experience estrus (Gangestad and

Thornhill 2008) is at odds with the demonstrable difficulty of detecting ovula-
tion in women. Until the 1920s, even medical experts believed that ovulation
occurred during menstruation rather than at midcycle (Strassmann 1996). In a
cross-cultural sample of 186 preindustrial societies, I confirmed an earlier report
by Paige and Paige (1981) that the most prevalent belief was that conception occurs
immediately after menstruation—a view also supported by in-depth field studies
of the Dogon of Mali (Strassmann 1996) and Hadza foragers of Tanzania (Marlowe
2004). Needless to say, no man can point to the ovulating women in the room with
any appreciable success.
A careful study of American women by Sievert and Dubois (2005) asked: Do
women who think they know when they ovulate truly make accurate assess-
ments? Women collected daily urine samples from day 5 of the menstrual cycle
through the day they believed they ovulated. The last three samples were tested
for a luteinizing hormone (LH) surge and if at least one sample tested positive
for an LH surge, then that woman was scored as correct in her assessment for
that cycle. To detect ovulation, the women most frequently relied upon changes
in cervical mucus (“spinnbarkeit”), abdominal pain (“mittelshmertz”), and the
expectation that ovulation occurs at midcycle—such information derives from
modern medical research to which ancestral women would not have been privy.
Using these signals, only 28% of women who believed that they knew when they
ovulated actually gave accurate assessments. When the analysis included women
who used basal body temperature as an assessment technique, the accuracy rate
went up to 36.1%. These results suggest that even in the presence of contempo-
rary medical information, ovulation is concealed for most women (Sievert and
Dubois 2005).
 Kinship, Parental Care, and Human Societies } 143

The inaccuracy of self-reports of ovulation does not preclude the possibility

of subtle changes across the menstrual cycle in women’s sexuality, and identify-
ing such changes has become a particularly active area of research in evolution-
ary psychology. A recent review concludes that ovulation cues can be found in
women’s social behaviors, body scents, voices, and possibly, aspects of physical
beauty with effect sizes ranging from small (d = 0.12) to large (d = 1.20) (Haselton
and Gildersleeve 2011, see also Alvergne and Lummaa 2009).
Most studies in this arena are based on the hypothesis that psychological adap-
tations should differ when a woman is in the ovulatory phase of the menstrual cycle
versus when she is not. The investigators then proceed to document differences in
lap dance tips, vocal attractiveness, and other outcome variables at “fertile” versus
“infertile” cycle phases. Upon finding differences, the investigators then assume
that they have found support for their adaptive hypotheses about male and female
sexual strategies. Although this is a burgeoning literature, few studies (Puts 2006,
Welling et al. 2007, Roney and Simmons 2008) concern themselves with examin-
ing the underlying mechanisms. As Gangestad and Thornhill (2008, p. 997) noted:
“The precise endocrine mechanisms that regulate these changes remain largely
unknown.”
At present, there are no hormones that are strong candidates for explaining the
reported ovulation cues. Testosterone contributes to libido in women (Wylie et al.
2010) and therefore might be a hormone of interest. In a recent study (Rothman
et al. 2011), however, the difference in serum testosterone and free testosterone
between the midcycle and midluteal phases of the menstrual cycle was small and
not statistically significant. Estradiol and estrone are other hormones of possible
interest, but it is androgens and not estrogens that are prescribed to increase libido
in women (Schwenkhagen and Studd 2009). Like the androgens, the estrogens are
elevated at both midcycle and the mid-luteal phase (Rothman et al. 2011). A hor-
mone that displays a sharp midcycle peak and is not elevated during the luteal
phase would be a stronger candidate for explaining behavioral changes that occur
only during or immediately prior to ovulation. Although luteinizing hormone
might qualify, it has not (to my knowledge) been reported to influence behavior
in humans. If a hormonal basis for ovulatory cues is found, it will be necessary
to rule out the possibility that the cues are merely sideeffects rather than evolved
mechanisms that promote adaptive strategies (see Haselton and Gildersleeve 2011).
Researchers have not set forth their standards of evidence for detecting adaptive
design in the observed menstrual cycle correlates (see Reeve and Sherman 1993).
Instead they assume that if changes are detected in outcome variables at “fertile”
and “infertile” phases of the menstrual cycle, that this evidence alone is sufficient
to document psychological adaptations.
When studies of ovulatory cues involve surveys, exceptional diligence is needed
to prevent subjects from intuiting that the researcher’s focus is on the menstrual
cycle, as that knowledge could influence women’s responses. Such cueing from the
researcher can be extremely subtle, as demonstrated in a study in which subjects
144 { Human Social Evolution

read a newspaper article about a mass murder and were asked about the precipitat-
ing causes. The respondents’ answers were subconsciously influenced by the ques-
tionnaire’s fictitious letterhead. When the letterhead said “Institute for Personality
Research” respondents emphasized personality variables, whereas they identified
social-contextual variables when it said “Institute for Social Research” (Norenzayan
and Schwartz 1999). In a classic study, women who were manipulated by experi-
menters into believing that they were premenstrual reported experiencing a sig-
nificantly higher degree of physical symptoms, such as water retention, than did
women who were led to believe that they were intermenstrual (Ruble 1977). In
any research involving self-reports, it is challenging to prevent the questions from
shaping the answers (Schwartz 2010); researchers of ovulatory cues should address
this problem up front.
Laeng and Falkenberg’s (2007) study of female sexual response at three phases
of the menstrual cycle is noteworthy because it employed pupillary size as an index
of ”interest.” Changes in pupil size are not under conscious influence and do not
rely on responses to questionnaires, diaries, or ratings that might reflect partici-
pants’ beliefs. In this study, women’s pupils got larger during the ovulatory phase
of the menstrual cycle when they viewed photographs of their boyfriends but not
when they viewed the boyfriends of other subjects, or if they used oral contracep-
tives. I wonder what results might be obtained if women were asked to view pho-
tos of dogs (own dog, random dog) to further control for recognition effects and
non-sexual responses. In the sex research literature, female sexual response did
not change over the menstrual cycle as measured by vaginal blood volume, vagi-
nal pulse amplitude, labial temperature, and so forth (summarized in Laeng and
Falkenberg 2007). International data from the Demographic and Health Surveys
showed no evidence for a peak in coitus at midcycle for couples in stable unions
(Brewis and Meyer 2005). At best, the data are conflicting.
If there are indeed “ovulatory cues” in humans, then it should be possible to
document the mechanistic basis for the cues. Given the absence of evidence for the
underlying mechanisms, it is premature to claim that women possess psychological
adaptations surrounding mating that take account of whether they are ovulating
or that men shift their behavior in response to subtle ovulatory cues emitted by
women (Haselton and Gildersleeve 2011). Not only is the mechanistic basis for the
notion of “human estrus” or “ovulation cues” insubstantial, the theoretical basis
is also highly problematic. To make this argument, I turn to evidence from the
Dogon of Mali.

MENSTRUAL CYCLES IN THE DOGON OF MALI

Having experienced the difficulty of testing hypotheses on the evolution of con-

cealed ovulation, I was motivated to do my Ph.D. on questions about human
reproductive behavior that could be addressed empirically. I entered a Ph.D. pro-
gram in biology at Cornell University where key faculty disallowed research on
 Kinship, Parental Care, and Human Societies } 145

humans and where one professor informed me that I was, in his view, incapable
of doing fieldwork in Africa. To solve this problem, I returned to Michigan, where
I knew that I could count on Richard Alexander’s unflinching support. A great
aspect of Alexander’s mentoring is that he gave students free reign to develop their
own projects—those who did not like this system called it “sink or swim.” For
several months I sifted through library books about traditional peoples, eventually
choosing the Dogon after learning about them in the Time-Life series Peoples of
the Wild (Pern 1982). The Dogon had all the features I was looking for: menstrual
huts, no contraception, polygyny, nucleated villages, and an indigenous religion
that had not been fully supplanted by a world religion. My dissertation focused
on: (1) the biology of menstruation, (2) the function of menstrual taboos, and (3)
variation in female fecundability (Strassmann 1990).
In the mid-eighties, there was no previous, long-term, prospective study of
menstrual cycles in a population that was experiencing natural fertility. Whereas
North American women have about 400 menses during their lifetimes, Dogon
women in my data set had about 100 menses, most of which occurred in women
too young or too old to become pregnant. Repeated menstrual cycles were char-
acteristic of subfecund and infertile women. By contrast, women between the ages
of 20 and 35 years spent most of their time pregnant or in lactational amenor-
rhea—for these women, menstruation and ovulation were extremely rare events
(Strassmann 1997, Strassmann & Warner 1998). To take women’s evolved repro-
ductive biology into account, evolutionary psychologists should sample women
during all phases of the interbirth interval (pregnancy, lactational amenorrhea,
and menstrual cycling). Studies that are restricted to undergraduate women who
report regular menstrual cycles are not well suited for testing adaptive hypotheses.
Evidence from the Dogon is also pertinent to the theoretical expectation that
females engage in a dual mating strategy, seeking good genes from extra pair cop-
ulation (EPC) during ovulation while limiting threats to paternal care by remain-
ing faithful to their partners at other stages of the menstrual cycle (Symons 1979,
Benshoof and Thornhill 1979, Gangestad et al. 2002). If Dogon females were prone
to a dual mating strategy in which they sought EPCs during ovulation, then their
rate of extra pair paternity (EPP) should be much higher than it is. The rate of
EPP in the Dogon is 1.8% (N = 1704 father-offspring pairs), suggesting that in this
traditional society EPCs are rare—at least during the fertile period. Menstrual huts
are a cultural feature of Dogon society that helps to prevent cuckoldry by forcing
females to disclose the onset of pregnancy and the resumption of fertility after lac-
tational amenorrhea (Strassmann 1992, 1996). Extra pair paternity was more than
two-fold higher when the menstrual taboos were not enforced versus when they
had been abandoned, a situation associated with religious conversion (Strassmann
et al. 2012). Menstrual taboos were found in most pre-industrial societies and are
not unique to the Dogon (Strassmann 1992). They are a cultural tactic enforced
by males that helps to circumvent the concealment of ovulation (Strassmann
1992, 1996).
146 { Human Social Evolution

With the possible exception of the Jewish Halakha laws (Boster et al. 1998),
males do not use menstrual huts or other menstrual taboos to count to day 14 or
to identify the precise timing of the fertile period of the menstrual cycle. When
lactational amenorrhea lasts about 20 months—as in the Dogon—knowing that
a woman has resumed menstrual cycling provides strong evidence that she will
soon be fertilizable and must be mate-guarded (Strassmann 1996). Hormonal data
show that the postpartum resumption of the menses is closely tied to the resump-
tion of ovulation (Howie et al. 1982). Sometimes ovulation occurs first, other times
menstruation is first—either way the two events are usually only about two weeks
apart, which is minimal compared with the previous two-and-a-half years when
the woman was not fertilizable. The evidence for widespread menstrual taboos
in conjunction with the pervasive misimpression that the fertile period occurs
immediately after menstruation, suggests that: (1) human males are greatly con-
cerned about their risk for cuckoldry, and (2) their strategies usually do not pre-
cisely pinpoint the fertile period within the menstrual cycle.
Notwithstanding some fanciful accounts, it was males who imposed the taboos
on females in every society in which menstrual taboos were directly observed by
the ethnographer (Strassmann 1992). When females can successfully hide their
menses, then they can avoid more intensive mate guarding when they are cycling,
which may free them to copulate with extra-pair partners. They can also keep
greater control over knowledge of the genetic father’s possible identity. In soci-
eties as diverse as the Inuit of the Arctic (Balikci 1970) and the Dogon of Mali
(Strassmann 1992, 1996), fear that females might hide their menses was a major
male concern. When a woman is forced to obey menstrual taboos, then her repro-
ductive strategies are constrained—the husband and his family have the same
knowledge that she has about the timing of the menses and in the absence of
genetic data, this knowledge is important for paternity assessments (Strassmann
1992, 1996). Hormonal data show that menstrual hut visitation is an honest sig-
nal of menstruation in Dogon women of reproductive age (Strassmann 1996). If
women want paternal care for their offspring, and to bear sons who stand a chance
of being accepted into their social father’s patrilineage, then they must signal men-
struation honestly. In the Dogon, there is usually one menstrual hut and one shade
shelter for each patrilineage—the two structures are placed in close proximity to
each other so that the women at the menstrual hut can be monitored. Menstrual
taboos are embedded in religion because in all societies religions play a major
role in enforcing sexual morality (Strassmann et al. 2012). The addition of super-
natural threats to social norms is aimed at increasing compliance with the taboos
(Strassmann 1992, 1996).
In sum, females may benefit from EPCs, but they cannot engage in them with-
out risking the loss of paternal investment. When Dogon women divorce, they
do so immediately after leaving the menstrual hut because at that time they are
demonstrably nonpregnant (Strassmann 1992, 1996). In contrast with the report
that American undergraduate men are more proprietary toward partners who
 Kinship, Parental Care, and Human Societies } 147

are near ovulation (Gangestad et al. 2002), mate guarding in the Dogon is said
to be more intensive immediately after the menses—the time when the Dogon
believe that females are most fertile and are most prone to deserting their mates
(Strassmann 1992, 1996). I would expect that due to the riskiness of EPCs, women
usually seek to package “good genes” and paternal investment together in one
man at a time—as best they can. When the man proves deficient in either regard,
then women can use EPCs as a strategy for securing another combination pack-
age with a different (hopefully better) man. I present this “combo hypothesis” as
an alternative to the “dual mating hypothesis” which holds that EPCs are timed to
occur during ovulation. The “combo hypothesis” unlike the “dual mating hypoth-
esis” predicts relatively high paternity certainty in humans and low levels of sperm
competition.
Aside from the Dogon, the only genetic data on paternity certainty in a tra-
ditional, small-scale society come from a study of the Yanomamo of Brazil and
Venezuela. In this study, the EPP rate was 9.1% in a sample of 132 offspring (Neel
and Weiss 1975). A survey of 67 genetic studies reported that the median EPP
rate was 1.7% (range 0.4-11.8) for men who were not sampled at paternity test-
ing laboratories (Anderson 2006). Another review of the literature concluded that
EPP rates are around 2% in Europe and North America (Simmons et al. 2004).
Together with the Dogon result, there is emerging evidence for high paternity cer-
tainty in many human populations.
The diverse morphology of spermatozoa in human semen samples and the
low quality of human semen samples (Cooper et al. 2010) are indicative of a spe-
cies in which postcopulatory sexual selection was minor or even trivial. Species
with a high degree of postcopulatory sexual selection have reduced variation in
sperm morphology (Calhim et al. 2007, Kleven et al. 2008) and a high percent-
age of motile sperm per ejaculate (Møller 1988, Pizzari and Parker 2009). Human
semen samples do have some features in common with those of chimpanzees (Pan
troglodytes), but the evidence points to far less sperm competition in humans
(Anderson et al. 2007, Simmons et al. 2004). Chimpanzees have higher sperm
numbers, a reduced duration of epididymal transit, and the ability to maintain
high sperm counts in successive ejaculates (Marson et al. 1991, Anderson et al.
2007). Chimpanzee spermatozoa also have a higher mitochondrial membrane
potential which may improve sperm swimming speed or longevity (Anderson
et al. 2007).
For humans, the ratio of testes mass to body mass (0.06) is similar to that of
orangutans (Pongo pygmaeus) (0.05), three times that of gorillas (Gorilla gorilla)
(0.02), and 22% that of chimpanzees (Pan troglodytes) (0.27) (Harcourt et al. 1981).
Gorillas usually (but not always) live in single-male groups with only one sexu-
ally active male (Harrison and Chivers 2007) whereas chimpanzees live in multi-
male groups and have a promiscuous breeding system (Wroblewski et al. 2009).
Orangutans have a dispersed harem polygynous social system in which there are
two adult male morphs (flanged and unflanged); females prefer to mate with the
148 { Human Social Evolution

flanged males during the periovulatory period and flanged males sire most (but
not all) of the offspring (Harrison and Chivers 2007, Stumpf et al. 2008). Although
the ejaculates of chimps and orangutans are similar in volume, orangutans have
only one-tenth the sperm concentration (Graham 1988). The ratio of seminiferous
tubules to connective tissue in human testes is 1.3—similar to that of monogamous
gibbons (1.1), but far smaller than that of the primates with multi-male breed-
ing systems: chimpanzees (2.4), baboons (Papio) (2.8), and macaques (Macaca)
(2.2) (Schultz 1938, Harcourt et al. 1981). Thus, several lines of evidence suggest
that postcopulatory sexual selection has been relatively weak in humans, casting
doubt on the hypothesis that women have an evolved tendency to seek EPCs dur-
ing ovulation.
Alexander and Noonan’s hypothesis on concealed ovulation has been chal-
lenged by studies that report that the sexual strategies of men and women are
contingent on phase of the menstrual cycle—fertile or infertile (Haselton and
Gildersleeve 2011, Gangestad and Thornhill 2008). I have outlined several reasons
for being skeptical of these reports: (1) the high level of paternal investment that
characterizes most human populations is incompatible with high levels of cuck-
oldry, (2) genetic studies show relatively high paternity certainty compared with
the levels predicted by the “dual mating strategy” hypothesis, (3) morphological
and physiological comparisons of humans with other primates do not provide
evidence for postcopulatory sexual selection, (4) ethnographic and demographic
studies show that ovulation is indeed concealed, and (5) the mechanistic basis for
ovulation cues has not been identified. It is an honor to introduce Alexander and
Noonan’s chapter on concealed ovulation, as it sparked in me a lifelong interest
in the divergent strategies of males and females, and in the reproductive events
of menstruation, ovulation, fertility, and cuckoldry. It is a classic article, and with
each reading I notice something new.

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 CONCEALMENT OF OVULATION, PARENTAL CARE,
AND HUMAN SOCIAL EVOLUTION

Excerpt from Alexander, R.D. and Noonan, K.M. 1979. Concealment of

ovulation, parental care, and human social evolution. In N.A. Chagnon and
W.G. Irons (eds.), Evolutionary Biology and Human Social Behavior: An
Anthropological Perspective. North Scituate, MA: Duxbury Press.

Alexander et al. (this volume, chapter 15) describe reasons for assuming, from
its current attributes, that the human species has been polygynous during much
of its recent evolutionary history (i.e., that, generally speaking, fewer males than
females have contributed genetically to each generation, although not necessar-
ily that harems have been involved). Considerable evidence already indicates that
humans have essentially always lived in bands of close kin, probably containing
more than a single adult male (e.g., Lee and DeVore 1968). These two characteris-
tics, however, fit a large number of nonhuman primate species. Alone they tell us
nothing about how the human species came to possess its numerous distinctive
and social attributes.
Here we approach this question by first listing and discussing a number of
distinctive human attributes. Surprisingly, most of these attributes are sexually
asymmetrical or involve the interactions of the sexes. They suggest that the human
male is not particularly unusual among primate males, except that he is generally
more parental than the males of other group-living species. On the other hand, the
human female is distinctive in several regards, most dramatically in undergoing
menopause and in the concealment of ovulation. Menopause has been associated
with parental care by the female (Williams 1957; Alexander 1974; Dawkins 1976),
and we shall argue that concealment of ovulation is associated with the unusual
amount of parental care by the male. Several other distinctively human attributes,
such as length of juvenile life and helplessness of young juveniles, indicate that an
increase in the prominence of parental care was one of the most dramatic changes
during evolution of the human line.
Concealment of ovulation, as a strategy for obtaining parental care, seems
likely to evolve only in certain kinds of social situations. We believe that by con-
sidering the nature of these situations, together with circumstances that could lead
to the evolution of increased parental care, it is possible to gain insights into the
very general question of how humans evolved their distinctive sexual and social
attributes.
 Kinship, Parental Care, and Human Societies } 153

Most lists of distinctively human attributes include, in some form, the following
and little else:
1. Consciousness (self-awareness)
2. Foresight (deliberate planning, hope, purpose, death-awareness)
3. Facility in the development and use of tools (implying consciousness
and foresight)
4. Facility in the use of language and symbols in communication (implying
consciousness and foresight)
5. Culture (a cumulative body of traditionally transmitted learning—
including language and tools, and involving the use of consciousness
and foresight)

As suggested by the parenthetical comments, these five attributes are closely

related to one another, perhaps inseparable. They are also not strictly comparable
to one another: thus, consciousness and foresight are aspects of the human capac-
ity for culture, while language and tools are simultaneously vehicles and aspects
of culture. Culture in turn, by its existence and nature, and through its changes,
becomes a central aspect of the environment in which the capacities of individuals
to acquire and use consciousness, foresight, and facility in the development and
use of language and tools have been selected.
Although these five attributes may once have been regarded as uniquely
human, it now seems likely that all occur in other primate species, and chim-
panzees alone may possess all five, though not in the form or to the degree that
they are expressed in humans (Lawick-Goodall 1967; Gallup 1970; Premack 1971;
Fouts 1973; Rumbaugh et al. 1973; Gardner and Gardner 1969, 1971; Mason 1976).
The problem in understanding this set of related attributes, and why humans
possess them, is to determine their relationship to the reproductive success of
individuals during human history, when the capacities and tendencies to express
them were originating and being elaborated. Despite the attention paid to them,
these attributes have not been extensively analyzed as contributors to reproduc-
tive success.
Numerous other traits are also distinctive to humans (d, in the list below) or
distinctively expressed in humans, as compared to their primate relatives (de).
They may be either cultural (c) or noncultural (nc) in origin, and universal (u) or
not universal (nu) among humans. We first list these additional attributes, then
discuss their significance in trying to reconstruct the evolutionary background
of human sociality. Our reason for presenting this list, in developing an argu-
ment about the relationship of parental care and the concealment of ovulation
during human social history, is to emphasize how many distinctive human attri-
butes are somehow sexually asymmetrical (as) rather than symmetrical (s) in
their expression (probably all but 6 and 30 in the following list), and how many
involve: (1) interactions of the sexes in connection with parental care (especially
9–16) and (2) group-living (especially 17–30). We shall argue that concealment
154 { Human Social Evolution

of ovulation could only evolve in a group-living situation in which the impor-

tance of parental care in offspring reproductive success was increasing, and that
these two circumstances together describe a large part of the uniqueness of the
social environment of humans during their divergence from other primates. We
make no pretense that the following list is a complete set of attributes unique to
humans.
6. Upright locomotion usual (de, nc, u, s)
7. Frontal copulation usual (de, c & nc, u, as)
8. Relative hairlessness (de, nc, u, as)
9. Longer juvenile life (d, nc, u, as)
10. Greater infantile helplessness (de, nc, u, as)
11. Parental care frequently extending into and even across the offspring’s
adult life (d, c, u?, as)
12. Unusually extensive paternal care for a group-living primate (de,
c?, nu?, as)
13. Concealed ovulation in females (sometimes described as continuous
sexual receptivity, continuous estrus, “sham” estrus, or lack of estrus
(d, nc, u, as)
14. Greater prominence of female orgasm (perhaps - but see Lancaster,
in press) (d, nc?, u, as)
15. Unusually copious menstrual discharge (d, nc, u, as)
16. Menopause (d, nc, u, as)
17. Close association of close kin of both sexes, sometimes throughout
adulthood (de, c, u?, as)
18. Extensive extrafamilial nepotism (de, c, u?, as)
19. Extensive extrafamilial mating restrictions (de, c, u?, as)
20. Socially imposed monogamy (d. c, nu, as)
21. Extreme flexibility in rates of forming and dissolving coalitions
(d, c, u, as)
22. Systems of laws imposed by the many (or powerful) against the few
(or weak) (d, c, nu, as)
23. Extensive, organized, intergroup aggression; war (d, c, u?, as)
24. Group-against-group competition in play (d, c, u?, as)
25. Ancestor worship (d, c, nu, as)
26. Political and other kinds of appointed, elected, or hereditarily
succeeding leaders (d, c, nu, as)
27. The concepts of gods and life-after-death (d, c, nu, as)
28. Organized religion (d, c, nu, as)
29. Nationalism; patriotism (d, c, nu, as)
30. Polities of thousands or millions of nuclear families (d, c, nu, s)
What challenges, in the form of differential reproduction, caused the emphasis
on (1) consciousness and foresight, (2) social living, and (3) parental activities,
 Kinship, Parental Care, and Human Societies } 155

revealed in the above list of human attributes (cultural and physiological)? If we

assume that the above combination of attributes arose as a result of physical or
nonhuman biotic selective forces, such as climate, predators, or food shortages,
then an evolutionary sequence diverging humans so far from other species in the
particular directions they have taken, with all the intermediate stages becoming
extinct, appears difficult to reconstruct (Alexander 1971). In the absence of any
clear evidence of a massively unique selective environment in these respects for
humans, we would have to postulate that our uniqueness as a prehuman primate
preadapted us to respond uniquely to some not-so-unique concatenation of envi-
ronmental conditions, thereby evolving humanness. We regard this hypothesis as
unlikely.
The alternative is that something about the evolving human species itself
explains the differential reproduction that led to the divergence of the human line,
and the extinction of close relatives along the way. This possibility is immediately
tantalizing, since it suggests a solution to the problem of human uniqueness. Once
set in motion, such a selective force could be self-propelling and, simultaneously,
capable of suppressing similar trends in closely related lines. It further implies a rea-
son for the continuing elaboration of cultural patterns, outracing genetic changes
so dramatically as to render them trivial in regard to rates of behavior change.
The attribute that could cause differential reproduction leading to human
uniqueness, we believe, is an increasing prominence of direct intergroup competi-
tion, leading to an overriding significance in balances of power among competing
social groups, in which social cooperativeness and eventually culture became the
chief vehicle of competition. The probable relevance of complex social compe-
tition to human intelligence, consciousness, and foresight—and elaborate social
tendencies—has been emphasized before (Darwin 1871; Keith 1949; Fisher 1958;
Alexander 1969, 1971, 1974, 1975a, 1975b, 1977a, 1978a, in press a; Bigelow 1969;
Alexander and Tinkle 1968; Carneiro 1970; Flannery 1972; Wilson 1973). Intergroup
competition has not, however, been linked to the human emphasis on parental
care or the unusual sexual attributes of humans.
If intergroup competition was a principal guiding force in human evolution
and if groups as a result grew in size and in social unity among the individuals
comprising them, then parental care would have increased in value in two gen-
eral ways. First, larger group sizes inevitably meant intensified competition for
resources within groups. Juveniles, lacking the strength and sophistication to
compete successfully for themselves, would have benefited increasingly from
parental protection and assistance in securing resources for growth and future
reproduction.
Second, the intensification of both within- and between-group competition
implies a growing conflict in individual reproductive strategies by pitting the value
of direct competition with other group members against potential gain from their
cooperation in inter-group competition (or within-group alliances). Individual
reproductive success would depend increasingly on making the right decisions
156 { Human Social Evolution

in complex social situations involving self, relatives, friends, and enemies. Critical
choices would be aided by experience, and an intimate knowledge of the particular
social environment. Parents who could impart to their offspring this information
and the social skills for using and expanding it, while providing guidance dur-
ing the vulnerable years of learning, would have realized increasing reproductive
advantages over parents who failed to so equip their offspring. Buffered against
physical and social disaster by parental protection, the human juvenile may have
evolved to abandon efforts at serious direct competition, becoming increasingly
helpless over longer periods, while evolving extraordinary abilities to absorb
and retain information and develop skills through attachment, identification,
imitation, and more formal learning in early years. In other words, because of
the existence of groups intensely competitive against one another, and because
of the complexity of social competition within groups evolving to be effective in
intergroup competition, the human species in some sense became its own most
important selective environment, and the pressure of evolutionary change focused
increasingly on parental care.
Tendencies to infanticide or enforced desertion of infants would benefit males
to the extent that such practices hastened ovulation in females and preserved
female reproductive effort for the male’s own offspring. The increased parental
care of human mothers, its greater duration, and the wider spacing of babies
associated with more intensive early parental care and infant helplessness would
enhance the benefits of infanticide and enforced desertion of children to males
acquiring females from other males. Thus, an important aspect of male parental
care may have been protection of the child against other group males competing
for the female as a reproductive resource. Observations by Bygott (1972) suggest
that if a chimpanzee mother with an infant joins a new group, the infant is vulner-
able to infanticide by group males. Accounts of men (or women) killing children
made fatherless by inter-community warfare and exchange of women, such as
among the Yanomarno (Biocca 1969), imply that this may have been an important
selective context for paternal care in human history as well, and another indirect
consequence of the extension of juvenile dependence.
In ancestral humans, then, an orphan, even at an advanced juvenile stage, was
probably doomed to social impotence and reproductive failure, if not pre-repro-
ductive death, unless it was a female old enough to interest a mature male; the
extremely derogatory connotation of words for “fatherless” juveniles in nontech-
nological societies supports this inference (see Alexander 1977a). On the other
hand, juveniles with powerful parents and other relatives must have been essen-
tially certain of high success. Indeed, the unstratified or egalitarian bands pre-
sumed to represent the ancestral kind of human sociality can almost be defined by
saying that in them the major resource by which reproductive competition could
be maximized is kinspeople (see also Chagnon chapter 14).
To clarify these circumstances we first examine the social situations in which
concealment of ovulation might evolve and compare the resulting model with
 Kinship, Parental Care, and Human Societies } 157

extant nonhuman primates, then consider the situations in which increases in

parental care leading to the human condition might be favored.

WHY CONCEAL OVULATION?

The human female has commonly been described as “continually sexually recep-
tive” because she may willingly mate at any time during the menstrual cycle (James
1971). Most other female mammals mate only during a brief estrus period occur-
ring around the ovulatory period. To refer to the human female’s sexual behav-
ior simply as “continuous receptivity,” however, seems a gross oversimplification.
First, this “receptivity” is unlike the relatively uninhibited receptivity of some
estrous female mammals, which may accept essentially any male. By comparison,
the human female’s behavior might best be described as a kind of selective or low-
key receptivity, commonly tuned to a single male, or at least to one male at a time.
From the point of view of males not bonded to a particular female, it might just
as well be termed “continuous nonreceptivity.” It is a truly remarkable attribute
of human females that their ovulation is often essentially impossible to detect,
even, in some cases, through medical technology (Sturgis and Pommerenke 1960;
Behrman 1960; Cohen and Hanken 1960).
Conditions in nonhuman primates that seem to approach those of the human
female are: (1) sham estrus in langurs (Blaffer Hrdy 1974, 1977), (2) sexual receptiv-
ity outside the ovulatory period, especially in rhesus (Loy 1970) and chimpanzees
(van Lawick-Goodall, 1971; Lancaster, in press, reviews other primate cases of mat-
ing outside the usual estrus period around ovulation), and (3) relatively few external
signs of ovulation in gibbons (Carpenter 1941), orangutans (Rijksen 1975), gorillas
(Schaller 1963; Hess 1973; Nadler 1975), and possibly bonnet macaques (Simonds
1965; Rahaman and Parthasarathy 1969; MacArthur et al. 1972). In the last case we
are assuming that advertisement of estrus by pheromones is not unusually exag-
gerated in species with few visual signs; any efforts to quantify advertisement of
estrus among species are necessarily restricted to visual signs because no effort has
been made to accomplish this with pheromones.
In nonhuman primates the general period of ovulation always appears to
be more or less dramatically signaled to males (even if only by pheromones or
other means not obvious to human observers). All of the nonhuman primates
in which females are known to show “pseudo-estrus” are group-living spe-
cies, while the least obvious signs of ovulation seem to occur in monogamous
species like gibbons, or polygynous species, like gorillas, which tend to live in
single-male bands. Human females are thus unique in that they give little or no
evidence of ovulation and may be receptive during any part of the ovulatory
cycle. Although some women have discovered ways to determine the time of
their own ovulation, it is clear that selection has reduced the obviousness of
ovulation during human evolution, apparently to women themselves as well as
to others.
158 { Human Social Evolution

Emphasis on the so-called continuous responsiveness of the human female, in

trying to model its history, has focused attention on the proximate effect that the
male is able to enjoy copulation more or less whenever he desires it. Thus, it has
been argued that sexual competition is reduced among human males, allowing
larger group sizes and more extensive cooperation (Etkin 1963; Washburn and
Lancaster 1968; Pfeiffer 1969), or, that females keep their males at home by sup-
plying constant sex (Washburn and DeVore 1961b; Campbell 1966; Morris 1967;
Crook 1972). Those approaches have not provoked explanations for the male’s
retaining his interest in frequent copulation with his mate when fertilization of
her ovum is unlikely—that is, when she is not ovulating or when she is pregnant.
Focusing on concealment of ovulation within the essentially continuous receptiv-
ity of the female, on the other hand, raises the question of the value to the female
of this concealment. Evidently it deceives all males in the female’s vicinity, both
those with whom she is copulating and those with whom she is not copulating.
Such deceit would be valuable to the female only if recognition of the ovulatory
period somehow caused males to gain at her expense. In the absence of parental
investment by males, advertisement of ovulation would both assure the female
of copulation at times appropriate to fertilization and increase the likelihood of
competition among males, thus increasing her likelihood of securing a male of
unusual competitive ability (e.g., Cox and Le Boeuf 1977). Concealment of ovu-
lation and more or less continuous receptivity would have little value in this
circumstance, although some tolerance of mating may be expected to appear if
male insistence was quite deleterious to resisting females (e.g., McKinney 1975, on
ducks). Conversely, if males invest parentally, sexual advertisement of ovulation
might cost a female her mate’s parental care in two ways: (1) by attracting compet-
ing males who threaten his confidence of paternity, and (2) by freeing him, after
a brief consort period, to seek copulations with other fertile females who would
compete later with her for his parental care.
We suggest that concealment of ovulation evolved in humans because it enabled
females to force desirable males into consort relationships long enough to reduce
their likelihood of success in seeking other matings, and simultaneously raised the
male’s confidence of paternity by failing to inform other, potentially competing
males of the timing of ovulation. If these events occurred in a situation in which
paternal care was valuable, but not sufficiently valuable to males to offset philan-
dering (Trivers 1972), and in which desertion was frequent when confidence of
paternity was low, they could tip the balance, making increased paternal invest-
ment profitable to males. This strategy would be most likely to be successful for
females perceived by males to be of unusual value as mates. Thus, its effectiveness
would have been magnified during human history first by abilities and tendencies
of males to kill or enforce abandonment of fatherless offspring, and, second, by the
rise of differences in heritable wealth and status.
To explore the significance of concealed ovulation, we shall now consider varia-
tions in the advertisement of ovulation among female primates living in different
 Kinship, Parental Care, and Human Societies } 159

kinds of social groups, which might be considered to parallel certain aspects of

the social environment in which human sexuality evolved. We shall begin with
the most monogamous forms, such as the white-handed gibbon. The male and
female form an isolated, territorial pair and raise their offspring alone. There are
indications that adults are hostile to strangers of the same sex, and their territo-
rial tendencies would seem to minimize direct sexual competition (Ellefson 1974).
Males are virtually certain of their paternity because, usually, no other males are
around to compromise it, and females are relatively free of competition from other
females for their mate’s parental care. It might be supposed that the human species
lived in this fashion during much of its evolutionary history, and that the so-called
continuous receptivity of the human female evolved because such females tended
to keep their husbands home while other husbands went roving, presumably to
satisfy persistent sexual cravings. Such an argument, however, does not describe
the behavior of modern gibbons, which mate only when the female ovulates, and
it is difficult to defend on a logical basis. If males that stayed at home, tending their
mates and their offspring, outreproduced faithless males, their doing so would
surely not depend on whether or not their mates provided them with constant sex.
Indeed, in such circumstances, constant sex would be no more than a useless and
potentially dangerous distraction from the business of staying alive and healthy
and rearing one’s offspring. Rather than being continuously receptive, females in
such families should evolve to be receptive only during a brief period associated
with ovulation—just long enough, in other words, to maximize the likelihood of
fertilization at the appropriate times. They should not be gaudy or extravagant
about their responsiveness, communicating no further than the mate. The male,
likewise, should evolve to be interested in sex only during the same period and
only with his mate. Gibbons, which appear to behave as these arguments suggest
they should, do not provide a suitable model for the history which determined the
nature of present human sexuality. Only if continuous sexuality in the male con-
sistently yielded opportunities for philandering should it be maintained by selec-
tion and defenses against philandering be evolved by females because of the value
of male parental effort; these conditions are likely only when families are either
polygynous or in relatively close proximity.
In orangutans one male often controls a territory containing more than one
female (Rijksen 1975). It is not clear how effectively such males exclude other males,
and males move about, sometimes in groups, and apparently rape females (Rijksen
1975; MacKinnon 1971). Females sometimes approach males for copulation and
are said to prefer “high-ranking” males (Rijksen 1975). Males evidently provide
no parental care. From these reports, we might predict that orangutan females
advertise ovulation more than gibbon females, and are sexually responsive only at
ovulation time. Females may also be receptive when approached by strange males,
if such males might benefit from killing an offspring sired by another male or
when resistance to rape would be detrimental (infanticide, however, has not been
observed in orangutans). To the extent that orangutan females select males, they
160 { Human Social Evolution

might profit from concealing ovulation altogether and ovulating reflexively. Males
would then gain by copulating with any available female whenever they could. But
the orangutan situation, which is still known only very sketchily, appears not to
have led to extensive male parental care, nor does it involve extensive group-living,
both of which seem essential to a model of human social and sexual history.
Considering single-male primate bands next, such as gorillas1, we might again
predict a relatively low rate of sexual activity, and a relatively nonobvious estrus
period. Although females in a band must compete with one another to some
extent for the single dominant male’s attention, male competition apparently con-
sists largely in securing and maintaining a harem of females. To the extent that this
is true, females would gain little by advertising estrus more than is necessary to
secure the male’s attention at ovulation time, unless other potentially better males
are constantly in range of their signals, and able to use them to usurp ownership of
the band. As with gibbons, the male’s confidence of paternity is probably high—at
least in species in which harems are held for long periods—and some paternal care
should thus be evident. Because males are essentially certain of their paternity,
females would gain little in terms of a larger share of paternal care by concealing
ovulation and prolonging receptivity. Sexual behavior in gorillas is indeed infre-
quent, estrus is not sharply advertised, and the silverback male’s evident willing-
ness to repel potential predators could be interpreted as paternal effort (Schaller
1963; Fossey 1970, 1971).
1. Although blackback, younger males occur with gorilla bands includ-
ing but one silverback male, and some bands have two silverback males,
we believe gorilla bands are appropriately termed single-male, or at least
are different from such species as chimpanzees, cynocephalus baboons, and
rhesus macaques, because of the evident dominance of one male and the fact
that one silverback male generally determines band movements (Schaller
1963: Fossey 1970, 1971). Harcourt, Stewart, and Fossey (1976) argue that
the dominant silverback gorilla male inhibits other males from mating more
effectively than do dominant baboon or chimpanzee males and suggest that
some blackbacks are offspring of the silverback male.
In multi-male bands of nonhuman primates one finds the most dramatic adver-
tisements of sexual receptivity, the most obvious and intense sexual competitive-
ness, and—aside from single-male harems for which ownership changes frequently
(e.g., langurs, Blaffer Hrdy 1974, 1977)2—the most striking cases of receptivity out-
side the ovulation period. In baboons, macaques, chimpanzees, and a few other
forms that live in multi-male troops, the females develop bright-colored swollen
rumps during estrus. It is difficult to explain these gaudy swellings except on the
assumption that females in such groups gain by competing for the attention of the
dominant males. Paternal care is evidently minimal in such groups, compared to
one-male bands and isolated monogamous pairs, and one apparent correlate is a
low confidence of paternity. The gaudy females appear to be competing for the
 Kinship, Parental Care, and Human Societies } 161

attention of the males most capable of physically monopolizing them at ovula-

tion. There is no necessary correlation between a male’s ability to monopolize a
female and his ability to provide paternal care; such a correlation might evolve, for
example, if females consistently gained from protection against predators (or other
males) during the period of sexual receptivity. If monopoly gives a male high con-
fidence of paternity, his willingness to invest parentally may be raised; in contrast,
if a female copulates with a subordinate male, and he is quickly supplanted after
copulation, neither male is likely to be willing to provide paternal care.
The trend in the three kinds of social situations just discussed—isolated, ter-
ritorial pairs, single-male bands, and multi-male bands—seems opposite to that
which gave rise to the human condition, at least in regard to advertisement of ovu-
lation by the females and the extent of paternal care. Yet it is commonly accepted
that humans evolved in multi-male bands. On the other hand, it is difficult to see
how concealment of ovulation could evolve in either isolated monogamous fami-
lies or single-male harem groups, since there would be no “extramarital” males
from which to conceal ovulation. Nor does the evolution of tendencies toward
regular and continual sexuality in mated human males and females seem likely in
either single-male groups or monogamous families unless takeovers by new males
occur frequently enough (Blaffer Hrdy 1974, 1977).
2. Langurs are probably most appropriately compared to multi-male
troops because their rapid changes of ownership by males, and the sham
estrus of females by which even pregnant females mate with the new owner
of a troop, suggest that rapid shifts of ownership are not a novel or recent
phenomenon, as has heen argued in criticisms of Blalfer Hrdy’s (1977) con-
clusions, presaged by Mohnot (1971) and Sugiyama (1967)—see Alexander
(1974).
It might be argued that humans were extensively group-living, or multi-male
in social structure, when the distinctive attributes of the human female evolved.
Perhaps our ancestors lived in isolated monogamous families or in single-male
harem-polygynous groups, with initially extensive male parental care followed by
expanded group size in response to predator pressure. For two reasons, this alterna-
tive seems a less likely route to human sociality than the prevalent view that pre-
humans lived in relatively large multi-male bands. First, humans are thought to
have evolved in open woodland or savannah (e.g., Lee and DeVore 1968; Kolata
1977) where, today, there are no monogamous primates and few single-male, harem-
polygynous ones. Moreover, primate species in such habitats today (e.g., langurs,
vervets, paras) show anti-predator behavior which seems counter to the trend in
human evolution-hiding, secretiveness, and little direct confrontation of predators.
Man’s most similar relatives, chimpanzees, which inhabit woodland and savannah,
have a multi-male, polygynous social structure. Second, the selective pressures
generally thought to have been important in human social evolution—coopera-
tive defense, hunting, and inter-group competition—favor group sizes probably
162 { Human Social Evolution

greater than one male and his harem. So, even if humans began in small harem
groups, they obviously (and probably early) achieved multi-male situations which
tend to threaten pair bonds. Cooperation by males against predators occurs both in
multi-male bands with harems (hamadryas and gelada baboons) and in so-called
“promiscuous” multi-male bands (cynocephalus baboons). In both types of social
structure a male’s confidence of paternity is threatened to some degree, probably
more in the latter case. In summary, we believe that two coincident circumstances
can explain the evolution of concealment of ovulation. The first is a social situation
in which females of reproductive age are not completely inaccessible to males other
than their mates or consorts (e.g., multi-male groups or defensible multi-female
territories). The second is a growing importance of parental care such that the value
to a female of a male’s prowess in monopolizing her at ovulation time would be
overshadowed by the value of male prowess and willingness as a providing or pro-
tective parent. Gradual evolution of concealment of ovulation by females behav-
ing so as to maximize their mate’s confidence of paternity—hence his likelihood
of behaving paternally—would with each step toward concealment improve the
female’s ability to secure her mate’s parental care. Because no male could tell when a
female was ovulating, only a male who tended her more or less continuously could
be sure of the paternity of her offspring. Occasional forced or clandestine matings
outside the pair bond, in the absence of information about ovulation, would have a
very low likelihood of resulting in pregnancy (e.g., Tietze 1960).
According to what sequence of changes might the human female have evolved
her current uniqueness in regard to the cycling of sexual receptivity and external
signs of ovulation? One might consider three possibilities: either (1) external evi-
dence of estrus diminished first, with receptivity later increasing in duration; (2)
receptivity became more or less continuous, with external evidence of ovulation
later diminishing; or (3) these two changes occurred together. Since we favor the
hypothesis of a human ancestor living in multi-male groups we tend initially to
eliminate the first of these three possibilities.
Presumably sham estrus, or receptivity outside the ovulatory period, is effec-
tive only if it actually mimics estrus. It can only do this by becoming elaborate like
true estrus, or by a reduction in the elaboration of true estrus. One might imagine
that females gained directly from damping signs of ovulation, if pairing and some
male parental behavior preceded concealment of ovulation, as they must have. In
an extensively group-living species, however, at this stage, opportunities for males
to be polygynous must have been numerous, detracting from the value of the pair
bond to males, but not to females. It is difficult to see how a female could keep her
mate by damping sexual signals. Rather, a gradual extension of signals beyond
the ovulatory period seems a more likely way to lure the male into giving more
parental care than he would give if he based his effort on a correct determination
of the time of ovulation.
Steep differentials in female quality would enhance the effectiveness of this
deception. The highest-quality females (in terms of ability to bear and rear
 Kinship, Parental Care, and Human Societies } 163

offspring, and, perhaps, to enhance their status or other correlates of reproduc-

tive success), would be in demand by the highest-quality males most prone to
polygyny; such females could afford to prolong estrus longer than others with-
out risk of desertion by the male. Low-quality females would be at least partially
excluded from mating with the highest quality males by this ploy. Competition for
matings by lower-quality males would be reduced (because top-quality males are
already committed), making concealment of ovulation advantageous to low-rank-
ing females in securing at least some parental care for their offspring. Once sham
estrus became prevalent, reduction of external signs of ovulation seems inevitable
if only on the basis of cost reduction. So we postulate that sham estrus evolved for
a time to mimic true estrus, and subsequently the elaborateness of both true and
sham estrus was reduced.
Bright sexual skins in hamadryas and gelada baboon females at first seem to
contradict our hypothesis because these species have harem-polygynous breeding
systems. Paternity is more certain here than in the promiscuous polygynous bands
of savannah baboons, and one might therefore expect the evolution of paternal
care and concealed ovulation in females. However, observations by Kummer
(1968b) suggest that hamadryas females, too, may be competing for the attention
of high-quality males. Although harem-masters do not fight over estrous females
or mate extra-maritally they do battle over anestrous females so that females occa-
sionally pass between harems. Females are more “spatially independent” while in
estrus, perhaps inviting competition between their harem-masters and extra-mar-
ital males, primarily bachelors. Fighting takes place frequently between harem-
masters and bachelors, and occasionally between two or more harem-masters.
Mating occurs in crowded areas near sleeping cliffs, and adulterous matings with
bachelors are common, reducing the confidence of parenthood of harem masters.
Males in this system provide little direct parental care to their offspring, and the
willingness of females to stray and mate with other males suggests that securing
the best possible mating is more central to their reproductive strategy than main-
taining a high confidence of paternity.

CONCEALED OVULATION AND RAPE

When females do not reveal their ovulations, unmated males no longer have the
opportunity to compete for ovulating females. If our interpretation that human
females are better viewed as continuously nonreceptive or continuously selectively
receptive is correct, then males not bonded to a female have no way of obtaining
reproductively effective matings except by increasing their numbers of matings,
more or less randomly with respect to ovulation. Moreover, since female recep-
tivity does not correlate with ovulation, there is no reason, except convenience
and lowered risk, for males to seek only receptive females. A forced mating might
even be as likely to lead to actual success in reproduction, since unwillingness
sometimes would imply a pair bond, hence the possibility of paternal care for the
164 { Human Social Evolution

resulting offspring from a cuckolded male. In this sense, then, concealed ovula-
tion and some aspects of rape in humans may be historically related. As females
evolved to deny males the opportunity to compete at ovulation time, copulation
with unwilling females became a feasible strategy for achieving some reproduc-
tion. A raped female, moreover, might sometimes lose too much by revealing the
event to her mate, and this would increase the likelihood of rapists’ going unpun-
ished. Compared to other primates, then, a mating with a willing human female is
less likely to lead to reproduction (because she is less likely than a willing nonhu-
man primate female to be ovulating). A mating with an unwilling female is more
likely to do so (because she is more likely than an unwilling nonhuman primate
female to be ovulating, also more likely to have a male who gives paternal care and
whom, on that account, she is unlikely to inform of the rape).
In many societies in which rape occurs rather frequently, women submit to
avoid being hurt and usually do not complain later (e.g., New Guinea: Matthiessen
1962; Kenya: LeVine 1977). Such rapes are not necessarily associated with psycho-
logical pathology in the males or murder, characteristic of a significant proportion
of rapes in the U.S. (but see Amir 1971). The association of rape with murder and
psychological pathology in males in the United States may reflect the severe pen-
alties traditionally incurred for violating socially imposed monogamy. Only the
most deprived males (in actuality or by delusion) would be inclined to behave as
though viewing rape as a viable reproductive strategy in relation to other repro-
ductive alternatives; having committed such a crime, fear of discovery might lead
such males to murder their victims—canceling any reproductive gain, but escap-
ing certain death if caught.

CONCEALED OVULATION AND FEMALE ORGASM

Female orgasm was once regarded as unique to humans. Although recent stud-
ies suggest that this is untrue (see review by Lancaster, in press) the frequency
of orgasm in the human female, and perhaps its intensity or outward signs, may
still be unique. To examine the significance of this situation we may note first that
orgasms in other primate females have been described in species such as rhesus
macaques which live in multi-male groups and rather consistently show sexual
receptivity outside the ovulatory period (Lindburg 1971).
Orgasm in the human female, and perhaps other primates as well, may increase
the likelihood of fertilization (Fox et al. 1970; but see Masters and Johnson 1966:
122-124). But when should there be external signs of orgasm? We suggest two pos-
sibilities: (1) orgasms may sometimes increase the likelihood of abortion, thus
decreasing the likelihood of paternity mistakes in some circumstances, and (2)
external signs of orgasm may communicate the female’s sexual satisfaction to the
male. In the latter case the apparent tendency of female orgasm, in humans at least,
to resemble male orgasm, in the apparent absence of a correlation with an event
paralleling release of gametes (Masters and Johnson 1966), may suggest (l) that the
 Kinship, Parental Care, and Human Societies } 165

correlation is to some extent with the pleasure or satisfaction of male orgasm to

the male (so that the external signs of a female’s orgasm suggest to the male plea-
sure on her part similar to his own), and (2) that this aspect of the female orgasm
may be a communicative device which tends to raise her male’s confidence that
the female is disinclined to seek sexual satisfaction with other males. To the extent
that this interpretation is correct, the obvious outward signs of female orgasms
should (1) mimic male orgasms and (2) frequently involve deception, with females
pretending to have orgasms when they do not. Moreover, both this function and
effects on likelihood of fertilization suggest that orgasms should (1) occur most
frequently in (a) deeply satisfying or long-term interactions with males commit-
ted to the female and her offspring (Gebhard 1966), and (b) with dominant males
or males with obviously superior ability to deliver parental benefits, and (2) occur
least frequently in brief or casual encounters, or in copulation with a partner
unsatisfactory in the above regards. All of these contingencies seem compatible
with what is known about orgasm in human females, while few of them seem
to characterize male orgasm. All appear to be consistent with the information
reported by Lancaster, except possibly for the suggestion that female macaques in
the laboratory achieve orgasms sooner if they have been deprived of sexual activ-
ity. According to our speculation, female orgasms would perhaps be more likely
in females trying to obtain or keep a “good” male, identified as a male with much
parental investment to offer. Thus, we believe that this feature of human female
sexuality too may be linked to male parental care and the threat of desertion.

PARENTAL CARE AND HAIRLESSNESS

A possible relationship exists between the relative hairlessness of humans and their
emphasis on parental care. In the several published arguments on this question it
seems to have been overlooked that the least hairy of all humans are their juveniles.
Hairlessness in young mammals otherwise seems to correlate with multiple births
and a helpless period in the nest. Humans may be the only mammal giving birth to
a naked single offspring. We suggest that the selective value of being a juvenile, or
of giving that impression, should be investigated in efforts to explain the gradual
evolution of hairlessness in humans, and its present distribution among humans
of different ages and sexes.

UPRIGHT LOCOMOTION AND PARENTAL CARE

Upright locomotion has been associated with the evolution of hunting and tool
use (Eirnerl and DeVore 1965; Morris 1967). Washburn and DeVore (1961b) sug-
gest that parental care may be implicated in the evolution of bipedalism, as well.
They argue that, as the human infant became more and more helpless, and the
human mother more hairless, the baby was no longer able to cling unassisted, as
nonhuman primate babies do from a few days after birth. Upright posture may, in
166 { Human Social Evolution

fact, have tended to evolve first in females in the context of carrying infants. If so,
then with the possible exception of frontal copulation (7) and unusually copious
menstrual discharge (25), all of the attributes which we have identified as uniquely
expressed in humans appear to be related in some rather direct fashion to parental
care and other forms of nepotism.

SELF-AWARENESS AND CONCEALED OVULATION

Whether or not the above hypotheses about concealed ovulation are precisely
correct, any argument from adaptiveness must take into account that the human
female has evolved to conceal her ovulation not only from others in her vicin-
ity but evidently from herself as well. The timing of her own ovulation is not
commonly a part of a woman’s conscious knowledge. Unless one assumes that
other primate females, such as chimpanzees, are also not aware of their exten-
sive behavioral and physiological changes at ovulation, this fact suggests that it
has somehow been reproductive for human females actually to lose awareness of
their own ovulation.
If disappearance of outward signs of ovulation was favored because they
deceived other individuals, suppression of self-awareness of ovulation, unless
merely incidental, may appropriately be hypothesized to have furthered the decep-
tion. What is implied is that social deception may sometimes be more successful if
the deceiver is unaware of it (Alexander 1975b). Evolutionists can scarcely fail to be
puzzled and intrigued that with all the complexity of human consciousness, and its
apparent pervasion of all of our social interactions, humans nevertheless express
surprise, disbelief, or even outright anger at the suggestion that their behavior has
evolved to maximize their genetic reproduction. Unless one rejects the primacy of
differential reproduction this response indicates that it has been advantageous for
us to think that we have other goals. Perhaps what has actually been advantageous
is for us to be able continually to deceive others in regard to the nature and extents
of our likely gains as a result of particular activities with effects on them. That is,
except for avowed enemies such as members of alien or competitive groups, it may
have been more detrimental, during human history, to us as individuals to have
others construe continually that our immediate motivations for each social act
were personal gains relative to those with whom we are interacting or for them to
know exactly how much we are likely to gain from the interaction. Yet these are the
precise criteria of success in differential reproduction.
It is difficult to avoid the conclusion that we are better at convincing others
that our acts are truly beneficial to them and theirs, as opposed to ourselves, if
we believe it ourselves. Righteousness is a valuable aid and effective deceiver.
Deliberate lying is notoriously difficult as a social strategy; we are extraordinarily
clever at detecting it, vindictive and grudge-holding in our response to it, and
much more likely to be fooled by the selfish person with a sincere belief in his own
altruism and integrity.
 Kinship, Parental Care, and Human Societies } 167

The ability to deceive, partly by self-deception as to motives, we here suggest

to be a central part of human sociality, and of consciousness and self-awareness
in the human individual (see also Alexander 1975a). Concealed ovulation we view
as a particularly powerful and instructive case of deception of others, linked with
self-deception and made more effective by it.*

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19:20–22.
8}

Human Childhood

The Ones Who Continue

to dream expect to be a part
of children growing up,
of savoring comfort and pain,
the sociality of love,
of meeting all those challenges of life,
that we would like to go on and on
because, of course, they
are, somehow, everything.
Alexander, 2011, p. 254
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 INTRODUCTION

Altriciality, Neoteny, and Pleiotropy

Paul W. Turke

BROKEN RULES AND DASHED HOPES

It is a perilous game for a cricket biologist to write about human evolution.
Anthropologists have claimed this topic, and we have rules.
The first rule is, if you must mention another animal make it a primate, prefer-
ably a nice, sexy, matriarchal one like the bonobo. The second rule is, “the stan-
dard model of evolution”—the one proposing that adaptive design is organized
primarily at the level of the individual, with the effect of producing self-interested
individuals—is surely inadequate for explaining ourselves.
Dick Alexander repeatedly breaks both rules in his “Uniquely Unique” paper.
Fly larvae (a.k.a. maggots) are brought into the mix, for example, and there is a
conspicuous absence of models (of the sort which are popular once again) claim-
ing that we’ve evolved to be selfless group benefactors via implausible forms of
group selection or fanciful cultural co-evolutionary effects. Instead, nepotism
(Hamilton, 1964) and social reciprocity (Trivers, 1971; Alexander 1974; 1987) are
said to be the key drivers of human within-group cooperation, and even more
perilously Alexander suggests that within-group cooperation facilitates out-group
competition of the nastiest sort.
The “Uniquely Unique” paper has additional problems. It is sweeping in scope,
which is not conducive to neat data tables and statistically significant p-values.
This leaves it open to supercilious sniping, which it has gotten, but, as Alexander
is aware, the price one pays for addressing a large and important topic is often just
that. He states up front that his goal is not to have the last word. Rather, he strives
to pull together a grand account of human evolution that passes the initial test of
having all of its component parts fit together; and he hopes aloud that it will stimu-
late others to formulate additions and improvements.
In the first respect, I see great success. I see a roadmap for understanding
human evolution that is far superior to anything that came before. In the second
respect, the rest of us have largely let him down. There are probably many rea-
sons for this (including offense taken over the aforementioned broken rules), but
the lack of a suitable target cannot be one of them. After all, he tells us pointedly
174 { Human Social Evolution

that his human hairlessness argument (pp. 26–29) is low-hanging fruit—ripe for
improvement, so to speak. Accordingly, I will devote my remaining space to this
most glaring problem, and to the related problem of altriciality.

ALTRICIALITY
Altriciality is a little known term outside of evolutionary biology. It refers to physi-
cal helplessness. Precociality is its antonym. Alexander points out that human
infants are extremely altricial—like maggots—and he carefully reviews the expla-
nations previously given for the evolution of altriciality in the various species in
which it is present. He finds much to agree with in these explanations, but he then
does what he has been very good at throughout his career: he generalizes.
The general adaptive explanation for the evolution of altriciality seems to
be this: to the extent that a juvenile is relieved of the necessity to protect
itself from extrinsic hostile forces of nature (such as predation), it is freed to
devote a greater proportion of its calories to improving its performance at
some later stages of juvenile life or to becoming a better adult. (p.24)
Alexander goes into considerable detail describing the circumstances that might
diminish the value of precociality in certain species, which in turn potentially
opens the door to altriciality. For example, since it is very difficult to make a
maggot nimble or fierce, why try? Resources are likely better spent on improving
feeding efficiency, he argues, because feeding is more in keeping with the gen-
eral character of maggots than nimbleness or fierceness. For hominins the general
argument is the same, but the specific argument is very different. He proposes that
early physical precociality is sacrificed for the sake of mental precociality, which
I believe makes good sense under the assumption that mental precociality is a cru-
cial primer for successful reproduction in the milieu of an ever-escalating social
competition which came to characterize hominins at some early point, and which
still characterizes us today.
In short, under Alexander’s model altriciality can replace precociality if it frees
up calories that can be used to sufficiently improve some later occurring function.
Tradeoffs of this sort bring to mind pleiotropy.

LIFE’S “HAIRIEST” PROBLEM: FUNCTION PORTENDS DYSFUNCTION

I learned most of what I know about pleiotropy from Alexander. All of his many
graduate students and postdocs would have heard him recite Dobzhansky’s dic-
tum, “heredity is particulate, but development is unitary” (cited in Wigglesworth,
1961:111); and they would have heard him interpret it to mean that all genes there-
fore are both pleiotropic and epistatic. It is difficult to know whether most biolo-
gists have embraced this conclusion (I suspect that many haven’t), but it is clear
that Alexander is not alone in recognizing that pleiotropic genes must at least be
 Human Childhood } 175

very common. Williams (1957), for example, made genes that have advantageous
effects early but deleterious effects late (i.e., antagonistic pleiotropic genes) the
centerpiece of his theory of the evolution of senescence, and he felt confident in
doing so not because he could identify even one such gene but because his under-
standing of how organisms allocate effort to different functions as they develop
convinced him of their ubiquity (cf. Williams, 1966). Shoring up this conviction,
Kirkwood and Rose (1991) have pointed out that any gene that diverts resources
from repair functions to immediately improve some other function (e.g., making
gametes, mating, caring for offspring) increases the risk of downstream dysfunc-
tion. Similarly, I have proposed that development itself is always antagonistically
pleiotropic, which if correct forces the conclusion that all of the specialized struc-
tures and functions that comprise all organisms—from bacteria to people—are
built from antagonistic pleiotropic genes (Turke, 2008; 2013).
Development is always antagonistically pleiotropic, I believe, because it is
always driven by differentiation, and differentiation always diminishes totipo-
tency. Thus, while damaged tissues or organs can be repaired to a point, or regen-
erated in toto in some instances with considerable effort and risk (by keeping
pluripotent cells on standby, or by dedifferentiating and then redifferentiating, as
plants sometimes do), there are limits to repair and regeneration, and the limits
are proportional to the degree of differentiation. I cannot, for example, regrow a
limb or a kidney because too many long and tortuous differentiation pathways
were traveled the first time I grew them. The only possibility I’m left with is to
regenerate them secondarily by combining one of my germ cells with someone
else’s to recreate the totipotency that I started with. This is the very same conun-
drum that Williams (1957) identifies at the beginning of his famous article on
senescence in which he points out that a capacity for complete, primary mor-
phogenesis is inexorably transformed into an inability to merely maintain what is
already formed. A fuller discussion cannot be given here, but this claim—that it
is more difficult to indefinitely maintain a differentiated structure than an undif-
ferentiated one—contributes to the decision to repair damage, or not to, which
in turn is the basis for the evolution of Weismann’s (1893) germ-soma distinction
(Turke, 2008; Chao, 2010). Germ of course is undifferentiated and maintained
indefinitely, whereas soma is differentiated and disposable (see, e.g., Kirkwood
and Cremer, 1982).
Thus, if development (via differentiation) does indeed portend dysfunction for
the reasons I have just outlined, we can conclude that the specialized adaptations
that produce precociality are, in every instance, built from antagonistic pleio-
tropic genes. Furthermore, the spread, persistence, and continued expression of
such genes depends on the persistence of circumstances that allow the positive
side of antagonistic pleiotropy to outweigh the negative, which in turn depends
on both the timing and magnitude of expressed effects (e.g. Hamilton, 1966).
From Alexander’s hypothesis, the absolute magnitude of the benefit that early
hominins derived from physical precociality began to decrease and continued
176 { Human Social Evolution

to do so because of technological advances, such as fire and improved weapons,

and because of changes in social organization, such as more committed fathers
and more alloparents (e.g., Hrdy, 2009). Simultaneously these technological and
social upgrades were increasing the proportion of individuals living to older ages,
which would have meant that adult hominins increasingly experienced the nega-
tive side of antagonistic pleiotropy, and because the usefulness of older adults was
increasing (see “Uniquely Unique,” p.14), the force of selection against the dys-
function of old age was almost certainly on the rise. Furthermore, as Alexander
emphasizes, changes in the social milieu of our ancestors were creating more
profitable uses for the calories that physical precociality requires. Thus, due to
this combination of changing circumstances a hypothetical tipping point was
reached in which the net effect of many of the genes that build physical precocial-
ity became negative.
Nevertheless, since extant humans and apes are genetically very similar, it
seems unlikely that hominin evolution led to the wholesale elimination of genes
for physical precociality. Rather, I suspect that we retain most such genes, but that
their expression has been silenced or at least dampened by a relatively small num-
ber of regulatory genes. Hormones are key mediators of such regulation, which
brings us to hairlessness.
Hormones are among the most important signaling agents that turn soft, pudgy,
unaggressive, hairless human infants into NFL linebackers, but they do so rather
slowly and with dampened effects in modern humans, relative to in extant apes and
presumably in apelike early hominins. To be relatively soft, pudgy, and hairless—
which even adult linebackers are compared to adult apes—is to be, in a word, neo-
tenic. I suggest, therefore, that the evolution of human neoteny (and hairlessness,
which is a key feature of our neoteny) can be explained as follows. Neoteny is the
proximate basis for altriciality—that is, it exists as a collection of physical traits that
result in physical helplessness. Neotenic features, including hairlessness, are exag-
gerated in young humans and persist into adulthood because regulatory genes slow
the production and effects of maturation hormones, this in turn dampens the early
expressions of the many antagonistic pleiotropic genes that contribute to physi-
cal precociality, and also dampens and delays the late deleterious effects of these
same antagonistic pleiotropic genes (examples and additional explanation, below).
Therefore, altriciality and neoteny manifest, saving calories, which, as Alexander
suggests, are then diverted to cognitive development, and delayed senescence also
manifests, which is directly advantageous in individuals that increasingly achieve
reproductive success through lifelong learning and age-related social connected-
ness. Thus, lifespan extension is a direct adaptive consequence of neoteny/altrici-
ality. It is also worth noting that essentially the same argument (only some of the
details differ) can be used to explain the neoteny/altriciality and extended lifespan
of some social insect queens (cf. Alexander et al., 1991).
Alexander anticipates part of my explanation for neoteny and hairlessness by
recognizing that both are part of a developmental process that results in altriciality
 Human Childhood } 177

(p.28). However, he believes that this proximate-level explanation is inadequate

or at least incomplete because it does not identify any directly adaptive functions
of neoteny and hairlessness. He is led to this conclusion, though, only because he
does not connect the argument to antagonistic pleiotropy, which means that he
also does not connect it to the directly adaptive outcome that neoteny confers by
delaying senescence. Without these connections, neoteny and the hairlessness that
it entails might indeed be seen as non-adaptive incidental effects.
Alexander mentions senescence theory, and its pleiotropic underpinnings
(p. 28), just as I do here, perhaps hinting that he has a sense of the importance
of these concepts to his overall hypothesis; but he does not, at least not explicitly,
draw from them the same implications that I do. Rather, he seems simply to be
illustrating awareness of the fact that non-adaptive traits can evolve and persist
due the inability of selection to remove them. He then moves on without further
discussion to propose that hairlessness is possibly adaptive by virtue of promot-
ing heat transfer from parents to young offspring. Alexander is not entirely con-
vinced by his own proposal, however, foremost because it leaves unanswered “why
older juveniles and adult humans are relatively hairless” (p.29). My extension of
his primary argument potentially solves this problem by suggesting that a neo-
tenic phenotype that extends into adulthood provides a “somatic environment”
conducive to diminished and delayed expression of negative (senescence-causing)
pleiotropic effects.
The previous sentence succinctly expresses the crux of my argument. Let me be
less succinct. According to Williams (1957:400), many genes will express “opposite
effects on fitness at different ages, or more accurately, in different somatic environ-
ments” (emphasis his). Two hypothetical examples illustrate how fitness effects
might flip from positive to negative in organisms such as apes and humans due to
changes in somatic environment that are relatable to neoteny and altriciality.

(1) Consider a gene for an enzyme which folds into a specific configu-
ration when it finds itself in a pristine cytoplasmic environment. As such, it
efficiently catalyzes a biochemical reaction that is required at all stages of the
life cycle. However, in the course of an individual’s physical maturation (with
its many metabolic requirements), cell cytoplasm inevitably changes—water
content often decreases, various metabolites build up or decline, glucose con-
centrations rise or fall, pH changes, oxidative and other damage occurs, etc.
These changes in somatic environment alter the enzyme’s folding pattern and
hence its final shape, which diminishes its function; as a result, an original
positive fitness effect eventually becomes negative.
The scenario just given is hypothetical insofar as it does not identify a
known gene or enzyme, but Shi et al. (2008) have identified actual enzymes
that change as described for the general reason I have suggested. For my
hypothetical enzyme, as well as Shi et al.’s real ones, what might slow the
change from positive to negative fitness effect? One obvious possibility
178 { Human Social Evolution

would be to slow the rate of physical maturation, which would extend the
duration of a neotenic-appearing phenotype and thus help to maintain a
pristine cytoplasmic environment; and as suggested earlier this could be
accomplished via mutation in relatively small numbers of regulatory genes.
(2) Consider a suite of hormones that increase leanness, muscle
strength, hair growth, and aggressiveness. These proximal effects give an
advantage in most types of physical competition, but they also lead to more
fighting, more wounds, and more infections. The net effect of this suite of
hormones is nonetheless positive in up-and-coming adolescents and young
adults, given their fully functional immune systems and peak ability to
regenerate damaged tissues, but becomes negative once tissue regeneration
and immune function begin to falter, as they inevitably do over time. What
might slow this transition? Down regulation of hormone production.
In the first example, the change from positive to negative fitness effect occurs
because of changes in somatic environment occurring at the level of cytoplasm
biochemistry. In the second example, more distal environmental factors come into
play—factors such as the likely outcome of fighting when the entire soma is in its
prime versus when it is in decline. Both examples illustrate Alexander’s claim that
all genes are both pleiotropic and epistatic (see above), and at the same time they
show how changes in somatic environment—that is, changes that increase and
extend neoteny—can alter gene expression in a manner that results in altriciality
and an extended lifespan. Such changes of course would likely be disfavored in
apes (because, as Alexander suggest, apes benefit greatly from physical precocial-
ity) and favored in hominins (because, as he also suggests, hominins don’t).
Some might wonder at this point whether hairlessness, specifically, could be
decoupled from neoteny? I suspect that it could be, but I cannot think of a rea-
son that would justify the effort, especially if hairlessness is even slightly benefi-
cial to infants for the reason Alexander has suggested. One might similarly ask
whether the lifespan extension that has occurred in hominins could have been
achieved without extending neoteny into adulthood? I cannot envision how, with-
out changes so extreme as to render us entirely different from what we are.

A (MOSTLY) FALSE RUMOR AND A FINAL SPECULATION

Many of the leading evolutionary biologists of the past half-century have from time
to time been rumored to be too gene-centered in their approach. To paraphrase Mark
Twain, such rumors are greatly exaggerated. George Williams, for example, who is
surely among this era’s most influential evolutionary biologists, and surely a target of
such rumors, was acutely aware of the role that environment plays in gene expression
as evidenced by the central importance he gave to what he called the “somatic envi-
ronment” in determining the fitness effects of pleiotropic genes (see Williams, 1957,
and above). Williams’ theory of senescence, as well as the whole of his work, greatly
 Human Childhood } 179

influenced Alexander and it is this particular perspective—that phenotypic effects

of a given gene manifest from interaction with an environment that is multilayered,
and in which the layers of importance may include everything from other co-resident
genes to the social environment—that has made Alexander particularly well suited
to unraveling the most unique of human traits, including our extreme physical altri-
ciality, mental precociality, and of course lifelong learning. It is this nuanced view of
development, a view that sees plasticity of response as the raison-d’être of phenotype,
that allowed Alexander to see as perhaps no one did before him that culture is noth-
ing other than the “cumulative effect of the inclusive fitness maximizing behavior . . . of
all humans who have ever lived” (Alexander, 1979:68); and it is also a view, imparted
to his students, with considerable back and forth, as I recall, that is yielding creative
solutions to a wide variety of extraordinarily difficult evolutionary problems (see, e.g.,
West-Eberhard, 2003; Crespi and Summers, 2005; Crespi, 2008; Sherman et al., 2008;
Betzig, 2009, 2010; Flinn et al., 2009; Frank and Crespi, 2011).
I’ll close with a speculation, which I think is appropriate in a volume dis-
cussing the collected works of Dick Alexander. A central tenet of the Medawar-
Williams theory of the evolution of senescence is that organ systems should
senesce in tandem. Thus, the human immune system, for example, should not
regularly fail ahead of cardiovascular, renal, respiratory, digestive, and neuro-
logical systems. However, equality in the timing of system failure does not imply
equality in the amount of effort that has been put into achieving in-tandem
senescence of vital systems. It is possible, in other words, that one system more
than others has been a limiting factor in the extension of the human lifespan to
a maximum of a little more than 100 years. In particular, from Alexander’s altri-
ciality hypothesis there is reason to suspect that maintaining cognitive function
to advanced ages has been an especially difficult feat to achieve. This follows
because although silencing or removing the genes for physical precociality
became an option during hominin evolution, quite the opposite is predicted for
genes contributing to enhanced cognitive ability in children and young adults.
These genes are likely to have been added and/or up-regulated during hominin
evolution, and if their late-life effects are detrimental to the central nervous
system—which is expected if diminished totipotency/regenerative capacity is,
as argued, the price individuals pay for enhanced early function—then the loss
of cognitive function will have been a long-running constraint on hominin
lifespan extension. Sadly, as health care, sanitation, and other modern inven-
tions keep more people alive longer, the devastating nature of this constraint is
becoming more and more apparent.

Acknowledgments

I thank Dick Alexander, Laura Betzig, Bernie Crespi, Bev Strassmann, and Kyle
Summers for a number of thoughtful suggestions.
180 { Human Social Evolution

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Alexander, R.D. 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5: 325–83.
Alexander, R.D. 1979. Darwinism and Human Affairs. Seattle: University of Washington
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Alexander, R.D. 1987. The Biology of Moral Systems. New York: Aldine-de Gruyter.
Alexander, R.D. 1990. How did humans evolve? Reflections on the uniquely unique species.
Univ. of Mich. Spec. Pub. 1:1–38.
Alexander, R.D., Noonan, K. M., and Crespi, B. J. 1991. The evolution of eusociality. In:
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Chao, L. 2010. A model for damage load and its implications for the evolution of aging.
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Crespi, B. 2008. Genomic imprinting in the development and evolution of psychotic spec-
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Crespi, B. and Summers, K. 2005. Evolutionary biology of cancer. Trends Ecol. Evol.
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anisms linking attachment and life history: the social neuroendocrinology of middle
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Frank, S.A. and Crepsi, B. J. 2011. Pathology from evolutionary conflict, with a theory of X
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Sci. USA 108 (Suppl. 2):10886–10893.
Hamilton, W.D. 1964. The genetical evolution of social behavior. J. Theoret. Biol. 7: 1–52.
Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theoret. Biol.
12(1):12–45.
Hrdy, S.B. 2009. Mothers and Others. Cambridge: HarvardUniversity Press.
Kirkwood, T.B.L. and Cremer, T. 1982. Cytogerontology since 1881: A reappraisal of August
Weismann and a review of modern progress. Hum. Genet. 60: 101–121.
Kirkwood, T.B.L. and Rose, M.R. 1991. Evolution of senescence: Late survival sacrificed for
reproduction. Phil. Trans. R. Soc. B, 332: 15–24.
Sherman, P.W., Holland, E. and Shellman Sherman, J. 2008. Allergies: Their role in cancer
prevention. Q. Rev. Biol. 83: 339–362.
Shi, J. Dertouzos, J., Gafni, A., Steel, D.G., and Palfey, B. A. 2006. Single-molecule kinetics
reveals signatures of half-sites reactivity in dihydroorotate dehydrogenase A catalysis.
Proc. Nat. Acad. Sci. USA, 103:5775–5780. PMID: 16585513.
Trivers, R.L. 1971. The evolution of reciprocal altruism. Q. Rev. Biol. 46: 35–57.
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West-Eberhard, M.J. 2003. Developmental Plasticity and Evolution. New York: Oxford
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 ALTRICIALLTY

Why Are Human Babies Helpless?

Excerpt from Alexander, R.D. How Did Humans Evolve? Reflections on a Uniquely
Unique Species. University of Michigan Museum of Zoology Special Publications
1:1-38.
Altriciality, or physical helplessness, is widespread among juvenile animals, but
the human neonate, which is distinctly more helpless than any of its primate rela-
tives, is probably the most famous of all altricial juveniles (Zeveloff and Boyce,
1980 and Dienske, 1986, survey an extensive literature). Although I concentrate
here on the human juvenile, I have tried to consider how to account for altriciality
wherever it occurs.
The words “altricial” and “precocial” are used primarily in the ornithologi-
cal literature and are defined in most dictionaries in terms of their application
to newly hatched birds (see also Gill, 1990). Altricial hatchlings, as with spar-
rows, starlings, and pigeons, are more or less naked and helpless; they may be
blind and are usually ectothermic. Food is brought to the nest for them by their
parents. In contrast, precocial hatchlings—as with chicks, ducklings, pheasants,
and quail—typically are covered with down, agile, homeothermic, have their
eyes open, and are more or less ready to move out alongside their mother and
pick up their food themselves. There are degrees of intermediacy (for example,
goslings are somewhat more helpless than ducklings, the eyes of owl hatchlings
are closed but not those of hawks, etc.). Gill (1990, pp. 369-70) exemplifies and
illustrates eight different categories of hatchlings originally established by Nice
(1962) based on “primary criteria of mobility, open or closed eyes, presence or
absence of down, and the nature of parental care. . . . ” The extreme differences
between (1) most songbirds and (2) mound-builders and most ducks, shorebirds,
and “fowl-like” birds is probably the reason why the terms altricial and precocial
were applied so readily to birds, as well as studied there more extensively than
in other organisms.
As Nice (1962) and Case (1978) noted, other animals also display variations
paralleling those found in birds. Newborn mice and rats are naked, blind, and
more or less helpless. They are born in a nest where they remain for some time.
In other mammals, such as some ungulates, on the other hand, newborn often
are able to stand alone within a few minutes, and some, such as horses, are able to
gallop alongside their mother in less than an hour. Newborn ungulates may travel
 Human Childhood } 183

considerable distances with their mothers, who are following a herd in more or
less normal movements. Again, there are intermediates: canine and feline babies
are blind when born but not naked, and not as helpless as most newborn rodents;
and some ungulate newborns are physically less capable than others.
It is useful to apply the concepts of altricial and precocial even more widely,
for example to insect juveniles. Maggots, and the maggot-like larvae of some
insects with complete metamorphosis (e.g., honeybees), can be regarded as altri-
cial (in a broader application of the term, so can all insect larvae). In contrast,
the nymphs of insects with incomplete metamorphosis, such as grasshoppers
and crickets, are precocial in the same sense as some baby mammals and birds.
Again, there are intermediates. For example, within the Family Gryllidae (Order
Orthoptera), including all crickets, most juveniles would be seen as precocial.
Their exoskeletons are hard, and they are agile, quick, and seek out their own food
right from hatching; there is no parent alive to assist them. But in genera such as
Anurogryllus, in which the female cricket prepares a closed burrow with a food
cache before she lays her eggs, and then tends her babies until she dies—feeding
them small, apparently unfertilized trophic eggs—the hatchlings are soft and fat,
resembling termite juveniles (West and Alexander, 1963). Many other examples
could be given: thus, caterpillars may be soft and helpless or quick-moving and
covered with urticaceous hairs or other defenses. Many internal parasites, espe-
cially those living in the alimentary tracts of their hosts, have some of the features
of altricial juveniles. Certain adult insects, such as queens in large-colony euso-
cial forms, possess some of the characteristics of altricial juveniles (Alexander
et al., 1991).
Ricklefs (1974, 1975, 1979a, 1979b, 1983) has contributed extensively to the
development of theory that helps explain altricial and precocial juveniles.
Initially he showed that altricial nestlings of birds grow faster than the more pre-
cocial nestlings of related species, and he eventually concluded (1983, pp. 11-12)
that “The overwhelming advantage to altricial development seems to be rapid
growth. . . . Although adoption of the altricial condition may increase vulnerability
to predation and enhance the effects of exposure to bad weather, these are presum-
ably more than compensated for by the brevity of the development period.” Faster
growth may actually be the adaptive function of altriciality in a wide variety of
species. The human embryo and neonate both grow faster than do the embryos
and neonates of their primate relatives (Sacher and Staffeldt, 1974). It is difficult to
believe, however, that this is the full explanation for the altriciality of the human
infant. Unlike altricial birds, for example, the human juvenile has a juvenile life as
long as or longer than those of the closest relatives of humans whose juveniles are
all less altricial (Smith, 1989). As Montagu (1961, p. 56) notes, “man is born and
remains more immature for a longer period than any other animal.”
Dienske (1986) has reviewed and criticized previous theories about human altri-
ciality, giving good reasons for doubting that human newborns are altricial simply
because more advanced neonates could not pass the pelvic passage, and pointing
184 { Human Social Evolution

out that although apes have pelvic passages that are larger in relation to their babies’
heads than are those of rhesus macaques, the apes’ babies are more altricial. It does
not seem likely either that the human baby is simply born at an earlier stage through
shortening of the gestation period, since the great apes have about the same ges-
tation periods as humans, or slightly shorter (Schultz, 1956; Sacher and Staffeldt,
1974), and the 12-month gestation briefly postulated for Neanderthals because of
a presumed larger pelvic opening has since been discounted (Rosenberg, 1986;
Greene and Sibley, 1986; Trevathan, 1987; Trinkaus, 1987). Dienske also doubted
that altriciality occurs because the human baby’s brain is small in size, since it is
comparable in size, in relation to the body weight, to that of other primates. Dienske
summarized the evidence that in humans the adult brain is much larger, in relation
to its size at birth, than those of other primates, and he wondered if this might not
have something to do with altriciality, supposing that this difference might mean
that the neonate’s brain is less developed. As he put it: a neonate brain that is smaller
in relation to the adult brain “ . . . implies a greater immaturity if many parts of the
neonatal brain are still in a (rudimentary) stage of functioning.” Although this
hypothesis is probably correct, it need not imply that this aspect of altriciality is
explainable simply as a result of a physiological or developmental constraint or that
human neonates are “embryos,” simply born at an earlier stage of development (e.g.,
Kuttner, 1960). That view would not account for the early mental precociality of the
human juvenile compared to ape juveniles or engage the question of the pattern of
development of function in the human brain.
Zeveloff and Boyce (1982) seek an adaptive hypothesis for human altricial-
ity. Concordant with the arguments developed here, they suggest (p. 540) that
“ . . . monogamous pair-bonds and concomitant opportunities for paternal invest-
ment may contribute to the evolution of human altriciality,” and that monogamy
and paternal care were made more likely by increased confidence of paternity.
They also argued that increased time for learning, from an increased length of
the juvenile period, is the main benefit of altriciality. My arguments here differ
from theirs in that (1) they sometimes seem to be suggesting that monogamy and
paternal care evolved because of altriciality (“an altricial neonate will offer greater
potential for male parental care ”- p. 537) rather than vice versa and (2) they seem
to assume that altriciality (a) depends on a shorter gestation period and (b) is
responsible for the longer learning period (see also Case, 1978; Zeveloff and Boyce,
1980). The extensiveness and profundity of learning and maturational changes in
human juveniles following ages 11–13 indicates that it is appropriate to refer to the
human juvenile period as lengthened in comparison to those of related primates
even if the earliest time of possible reproduction is about the same for chimpan-
zees and humans (Smith, 1989). This extended juvenile period may have evolved
for the same reasons as human neonate altriciality and not simply as a necessary or
incidental result of it—that is, because it contributed to the long learning period,
or period of plasticity, that enables human juveniles to absorb and cope with the
complexities of culture and human sociality.
 Human Childhood } 185

In general, we are not hard-pressed to provide adaptive hypotheses for pre-

cocial organisms having the attributes that cause us to label them as precocial. It
seems obvious why a baby ungulate would gain from being able to run alongside
its mother soon after birth. Precocial birds are often tended only by their mothers,
are usually hatched in vulnerable nests on the ground, and typically eat the kinds
of food that can be captured by moving about on the ground or in the water (Nice,
1962). Juvenile insects in species with incomplete or gradual metamorphosis (that
is, the precocial sort) live without parents in dangerous locations, and they are
usually able either to run or leap, or else they produce various kinds of poisons or
other deterrents to predators. Their abilities to do these things are what causes us
to see them as precocial. The same is true, more or less, of relatively precocial lar-
vae in insects with complete metamorphosis (that is, larvae with urticaceous hairs,
unusual locomotory abilities, or any other special defensive features), even though
the larva itself, and the form of metamorphosis (“complete”) that it typifies, can be
seen as an evolutionary trend toward an altricial feeding stage.
The question that remains is: Why, when extrinsic sources of mortality are
removed, do juveniles become soft, fat, helpless, and maggot-like? Is there a gen-
eral answer, other than the unsatisfying or incomplete one that particular selective
pressures are relieved or removed, or that there is some advantage to the parents
rather than to the juvenile itself? Case (1978), for example, offers several possibili-
ties for the latter, but all seem to depend on shorter gestation periods and young
being smaller in altricial forms. Although some cases of altriciality may fit one
or more of the arguments invoking advantages to parents, neither shorter gesta-
tion periods nor smaller young is always associated with altriciality; thus, altricial
neonates of humans are larger than less altricial neonates of their relatives (Sacher
and Staffeldt, 1974). Because some altricial organisms seem to have evolved
shorter juvenile periods (e.g., songbirds), and others longer juvenile periods (e.g.,
humans), any general explanation will have to take both conditions into account.
In seeking a broad explanation, we may first note that juvenile life has two main
functions: to get to the adult stage without dying and to become the best possible
adult. For our purposes the latter need have no more precise definition than to
be maximally capable of doing whatever an adult has to do in one’s own species
to reproduce as well as or better than anyone else. Presumably, the only selective
reason for the existence of a juvenile stage is that it gives rise to an adult that is
sufficiently better at reproducing to more than offset the disadvantages of juvenile
life such as longer generation time and investment of calories in other than repro-
duction per se.
The traits and tendencies that make one a better adult are not likely to be syn-
onymous with traits that enable one to bypass or deal successfully with particular
hazards along the pathway to adulthood. In other words, the two functions of
juvenile life are not likely to be achieved by precisely the same directions of selec-
tion. What we call precociality evidently represents expensive ways of dealing with
hazards that may terminate juvenile life—expensive in the sense that they interfere
186 { Human Social Evolution

with selection that otherwise could cause the juvenile to use more of its life effort
in preparing to be a more reproductive adult.
In the course of becoming satisfactory adults, juveniles must do two things:
grow and develop. Growth enables the juvenile to reach an appropriate adult size
at the appropriate time or season. Development, which can be defined as differ-
ential growth or change in different tissues or organs, involves changing from the
form or function that best serves the juvenile to that which best serves the adult.
But this description is still far too simple. Juvenile life is not necessarily unitary:
in different forms it can be subdivided into multiple stages, each of which takes its
own form, growth rate, developmental rate, and way of functioning. Obviously, all
of these things may be affected by changes in the nature or emphasis of the forces
that affect the juvenile’s success, such as sources of mortality.
Complex metamorphoses—as illustrated by parasites (especially those with
multiple hosts), anuran amphibians, and insects—presumably evolve when appro-
priate forms and functions for different stages of the life cycle vary widely. The lar-
val stage of insects with complete metamorphosis lives in habitats that are suited
to feeding and growth. Development is primarily restricted to the pupal stage,
which follows the larval stage. The adult does not resemble either of the two juve-
nile stages or, in general, live in the same habitat. A similar pattern is exhibited
by anuran amphibians, with the feeding, aquatic tadpole eventually transforming
during a relatively short period into an adult that is dramatically different in form
and function and lives in a different range of habitats.
Such patterning during the juvenile life may be considerably more subtle, yet
requires understanding if we are to explain the nature of the human juvenile
and the patterning of its life. Thus, the altricial juveniles of songbirds for the
most part live at first in a nest hidden from predators or inaccessible to them but
shortly become capable of flight and leave the nest (songbird nests must often
become increasingly vulnerable to predation as the juveniles grow and the par-
ents visit the nest increasingly frequently to feed them). Following fledging, the
juvenile songbird’s life soon becomes that of an independent flying bird which
lives more or less in the adult habitat. As Ricklefs (1983) specified, his description
of altriciality as a way of providing more calories for the growth process thus
applies only to the earliest part of juvenile life—the time spent in the nest. That
period, moreover, necessarily includes not only rapid growth but the develop-
ment required to transform an altricial hatchling into a feathered, coordinated
fledgling capable of flight and with keen sensory apparatus enabling it to avoid
predators and locate its own food. In precocial birds these parts of development
largely precede hatching. We are required to assume that altriciality, involving
only a brief initial part of a songbird’s juvenile life, provides sufficient advantage
in growth rate to more than compensate for the delay in initiating the dramatic
developmental changes necessary for transformation into a suitable fledgling,
which in at least some cases might appropriately be described as having achieved
a certain precociality.
 Human Childhood } 187

In some senses songbird hatchlings parallel certain altricial juvenile insects,

such as the fly larvae called maggots that occur in dung, carrion, fungi, and other
short-lived and vulnerable habitats. These larvae do not seem well protected from
predation, weather, or deterioration of their microhabitats. Why, then, do they
take on the aspect of being altricial? I would guess because they cannot do any-
thing about the serious threats in their habitat, so that their best strategy is to get
through the dangerous feeding stage and out of the larval habitat as fast as pos-
sible. As with internal parasites, who may be protected, their particular form of
altriciality has caused them to evolve to become mere “sacks” of efficient nutrition-
grabbing ability. In their temporary and dangerous hatchling environments they
load themselves with nutrients as fast as possible and drop off or crawl out of the
dangerous place where they have secured their food to grow and develop in safer
locations. One might suspect that they are highly precocial in terms of their ability
to ingest their medium rapidly.
Songbird and insect patterns of altriciality are not easily compared to those
of humans. First, neither songbird hatchlings nor maggots have evolved coin-
cidentally altriciality and a longer juvenile life as have humans. Second, unlike
songbirds, in humans parental care remains extensive not only throughout the
juvenile’s life but well into its adult life.
The general adaptive explanation for the evolution of altriciality seems to be
this: to the extent that a juvenile is relieved of the necessity, or any importance, of
evolving to protect itself from extrinsic hostile forces of nature (such as predation),
it is freed to devote a greater proportion of its calories to improving its perfor-
mance at some later stages of juvenile life or to becoming a better adult. This will
be true, regardless of the means by which the relief is effected, whether by direct
or continual parental solicitude or by having been placed in a safe location by a
now deceased or departed parent. It will also be true regardless of the means by
which the improved later performance is effected: whether primarily by growth
or development. Protected juveniles are also free to bring back into their juvenile
life—further in time and to a greater extent—traits, tendencies, and events (learn-
ing or practicing) that are devoted to enabling their survival or competition as
older juveniles or as adults.
On this hypothesis allowing more calories to be devoted to growth is, as Ricklefs
(1983) maintained, surely a widespread advantage of altriciality. In songbirds this
is possible because the nest is either hidden or off the ground and inaccessible to
predators, and because in general both parents provide food. In some rodents and
subterranean crickets, as well as larvae injected by their mothers into safe loca-
tions such as inside wood, parallels in degrees of security from predation and the
physical environment have evolved.
Prior to parturition the human embryo grows faster than do the embryos of
other primates (Sacher, 1975), and the neonate is considerably larger in both body
weight and brain weight (Sacher and Staffeldt, 1974). Accordingly, it seems pos-
sible that the altricial nature of the human neonate yields a significant part of its
188 { Human Social Evolution

advantage as an increase in growth rate during the embryonic stage. The human
brain, however, also changes in mass during postnatal juvenile life several times
as much as the brains of other primates (Sacher and Staffeldt, 1974). Postnatal
body size changes in primates are considerably more variable, with gorillas add-
ing much more to their mass than humans or other apes and humans adding
more than chimpanzees (Sacher and Staffeldt, 1974). Effects of early altriciality on
growth rates during juvenile life—even as a consequence of the unusual intensity
and duration of parental solicitude—thus do not seem likely to explain the distinc-
tiveness of the entire pattern of human development.
The overall problem in understanding the adaptiveness of altriciality and pre-
cociality is thus one of trade-offs between different life stages, whether similar or
different activities or structures are being compared. Precocial birds have larger
brains than altricial birds (Gill, 1990), but the altricial human infant’s brain is
larger than those of its less altricial relatives (Sacher and Staffeldt, 1974; Dienske,
1986). In birds, the larger brain of the precocial bird is presumably used to protect
it from predators and other more or less immediate threats—that is, to provide
it with skills that increase the likelihood it will reach the adult stage. In humans,
however, the size and construction of the neonate’s brain has likely evolved for a
different reason—in a way that enabled it eventually to develop into an extraor-
dinarily large and complex brain that functions primarily in the complex social
activities required for reproductive success in the adult stage.
I hypothesize, then, that early physical precociality has been sacrificed in human
juveniles partly in favor of later mental precociality. I suggest that early physi-
cal precociality was expendable because human parents became almost entirely
responsible for the survival of the juvenile to adulthood, and for its failure to sur-
vive when this outcome occurs. This responsibility could only evolve, of course,
if the parents were capable of giving sufficient parental care of the appropriate
type and if their interests very broadly overlapped those of the offspring. On this
theory, the characteristics of the brain of the human infant are investments toward
the development of a better adult (or late juvenile) brain and are less involved in
the survival of the (early) juvenile than the enlarged brain of a precocial bird or
other animal.
If the general idea about altriciality presented here is correct, then to under-
stand the altriciality of human babies thoroughly we will need to understand
what kinds of attributes make the best possible adult (or late juvenile) human.
I think the answer is, generally speaking, intelligence and social capability. If
Humphrey’s (1976) argument about the evolution of the human intellect is cor-
rect, we should expect the physically altricial human juvenile to become, at
some point, intellectually and socially precocial, as suggested by Alexander and
Noonan (1979) in their discussion of parental care and the concealment of ovula-
tion. We should expect that the juvenile human begins practicing to be socially
successful much earlier in life and on a much more massive scale early in life
than is possible for less altricial primate juveniles. I think that this prediction
 Human Childhood } 189

is consistent with the seemingly inordinate attention given by humans to the

concept of so-called intelligence quotients, with their connotation of intellectual
precociality, attempting to measure mental development, or “age,” in relation to
physical or chronological age. It is also consistent with the efforts of many human
parents to parade their offspring as socially and intellectually precocial. Many
aspects of human juvenile life also give the appearance of social-intellectual
precociality—such as early smiling, humor, language acquisition, and engage-
ment in reciprocity. Throughout human history even young adult humans prob-
ably depended on their parents and other relatives for success, emphasizing the
importance of considering that even aspects of early human juvenile life may
take their form and function because of events that will transpire many years
later in late juvenile or adult life.
I also think of humans as having brought far back into their juvenile life many
kinds or instances of social-intellectual-physical play, as practice, and of them hav-
ing done so as part of what we usually have termed evolving increasing degrees
of altriciality. I think as well that they have been able to do this because of the
dramatic increase in the amount and effectiveness of parental care during human
evolution. For humans, explicitly, it seems to me that the question is moot as to
what extent the general increase in parental care took place because it allowed
human juveniles to devote more calories to becoming better adults, and to what
extent it occurred because it literally saved juveniles from death, thereby inciden-
tally allowing the juveniles to devote more of their calories to becoming better
adults. In either case, my hypothesis requires that in young juvenile humans more
calories are now devoted to better performances later in life, including adult life,
and I think this means being socially more effectively cooperative as a way of being
reproductively more competitive, than was the case in the days of, say, Homo erec-
tus, or of species ancestral to Homo.
The intellectual-social precociality of the human juvenile was probably respon-
sible for two prominent evolutionary theorists, G. Evelyn Hutchinson (1965) and
George Williams (1966), making independently the intriguing suggestion that
the creative intellect of adult humans is an incidental effect of selection for high
intellectual capacity in juvenile humans. The only way this argument seems to
me to have credibility is if it is applied only to the late juvenile (or early adult)
stages, when juveniles are actually striving to enter the breeding population. Even
with this qualification, it seems to me that the length of adult human life and the
evidence of rather dramatic increases in control of resources during adulthood,
together with the fact that the juvenile survives and succeeds primarily at the
behest of its parents and other adult close relatives, tends to deny the argument
that human brain complexity functions primarily during juvenile life.
Discussion.—Altriciality apparently evolves, then, when an infant gives up on
protecting itself and turns its protection over more or less entirely to extrinsic
forces. This protection may come about through continued attention by the par-
ent or because the juvenile lives in a protected situation, where it may have been
190 { Human Social Evolution

placed by its parent. If the extrinsic force is long-term care by parents or a perma-
nently safe location, the offspring is also free to evolve an extended juvenile life, if
by this it improves its adult performance sufficiently to compensate the added time
and expense involved. Altriciality in some attributes may even evolve in an unsafe
situation if thereby the juvenile can grow at the fastest possible rate and escape
the unsafe situation. In such cases, obviously, juvenile life will decrease in dura-
tion. Or, as in the case of internal parasites protected by being inside their host or
eusocial queens protected by their workers and soldiers, physical “altriciality” may
continue for the entire life of the organism, in the interests of turning all effort
to activities more directly reproductive than (useless) protection. Although two
parents (or any tending parents) are not required for the evolution of altriciality,
biparental care is a common situation, explaining the association with monogamy
in birds and mammals.

HAIRLESSNESS IN LATE JUVENILE AND ADULT HUMANS

I have not taken up the question of why humans remain relatively hairless as juve-
niles and adults, and I confess that I do not have a convincing hypothesis. Nor,
evidently, does anyone else. Some comparative discussion around this question,
however, may be useful.
The argument has been made repeatedly that ‘‘. .. the evolution of human hair-
lessness was somehow associated with temperature regulation in a tropical envi-
ronment” (Kushlan, 1980, p. 727: see also Campbell, 1966; Leakey and Lewin, 1977).
Morris (1967) suggested that hairlessness enabled humans to lose heat more effi-
ciently, as when chasing large game. Schwartz and Rosenblum (1981, p. 10) noted
that “As the ratio of surface/volume decreases in a static series of adult primates,
the advantage of an insulating coat diminishes as well.” The human baby, however,
is both the smallest human and the least hairy, and the human female, smaller than
the male, is next. Neither juveniles nor females do much chasing of large game.
As Darwin (1871) noted “ ... other members of the order of primates, . . . although
inhabiting various hot regions, are well clothed with hair.” No other predator that
captures its prey after chases in the hot areas of the world has lost its hair. Nor
has any other species at all taken up the particular pattern of hairlessness that the
human species exhibits, in which there is (1) a single naked infant rather than a
litter of naked infants and (2) a naked infant that is carried as opposed to being
hidden in a nest or a marsupial pouch. It is at least possible that in the hominid
line a hairless baby evolved first, followed by older juveniles, the adult female, and
finally the adult male.
It has also been argued that humans lost their hair because parasites were such
a problem, but then we have to ask why parasites were more of a problem with
humans than with other species. None of these or other hypotheses given so far for
human hairlessness (clothing, fire, and shelter made hair superfluous: Glass, 1966;
early humans were aquatic: Napier, 1970; sexual selection, species identification,
 Human Childhood } 191

social appeasement, neoteny: Darwin, 1871; Keith, 1912; Guthrie, 1970; see also
Kushlan, 1980) seems to have gained much momentum.
It appears that other relatively hairless mammals have lost their hair for reasons
that cannot be used to explain human hairlessness. The following arguments on
this topic are modified from Alexander (1991b), a chapter written for a volume on
naked mole-rats. The prevalence of ectotherrny among altricial mammal and bird
juveniles, and the ability of human babies to survive extreme lowering of the body
temperature for long periods, suggest a general connection between ectothermy
and altriciality, and raise questions about the apparent connections between ecto-
thermy and nudity in some cases.
Mammalian Variations in Hairlessness.—Mammals are the organisms that have
hair and produce milk. There are analogues for both traits in other organisms
(pigeons produce a milk-like food for their young—see discussion in Gill, 1990—
and many organisms have hair-like structures), but no homologues.
The amount and kind of hair varies extensively among different mammals.
Relative hairlessness occurs in a variety of mammals, rarely for reasons that are
entirely obvious (Lyne and Short, 1965; W. J. Hamilton, 1973; Jarvis, 1981). For
some aquatic mammals, both marine and freshwater (e.g., cetaceans, sirenids),
a layer of fat beneath the skin seems to have proved a more appropriate correlate
of homeothermy than a coat of hair, partly because hair causes drag in an aquatic
environment, reducing the efficiency of locomotion, and partly because trapped
air in pelage or plumage can be lost through compression, for example as a result
of diving. Although a variety of aquatic mammals have retained a hair coat (seals,
walruses, polar bears, otters, mink, beaver), these seem invariably to be either spe-
cies that live in cold climates or species that spend a significant amount of time out
of the water. Some mammals have replaced part or all of the hair coat with armor
of one sort or another (armadillos, pangolins, ant-eaters—in some armadillos
abundant ventral hair is retained); such forms also live in mild or tropical climates
(Walker, 1975). Several large, entirely terrestrial (elephant, rhinocerus) or primar-
ily terrestrial (hippopotamus) mammals have lost a hair coat in favor of a thick,
leathery skin. It has been postulated that these tropical forms have a low body
surface area in relation to their body mass and therefore have gained by increasing
their ability to lose heat through the skin. As predicted from this hypothesis, tem-
perate zone, montane, and rain forest-dwelling relatives of these forms have more
hair, and juveniles of these forms have more hair than adults (Walker, 1975). A few
mammal species (suids and some primates) are somewhat intermediate, having
lost much of their hair (Lyne and Short, 1965). Many mammals that bed down or
nest in contact with their young, or carry infants on their venters, have lost much
of the hair on their venters and around the mammary glands (e.g., suids, rodents,
some primates). In such cases the young juveniles are also either virtually hair-
less (rodents), relatively so (suids), or only lightly haired on the particular parts
of their anatomy that regularly contact the mother (primates) (birds that brood
altricial young also sometimes have bare patches on their venters).
192 { Human Social Evolution

Only two mammal species additional to the above groups have virtually hair-
less adults and older juveniles: naked mole-rats and humans. Each of these species
appears to have evolved nudity independently of any other mammalian forms,
since their close relatives are all relatively hairy. The exception to this statement is
that nearly all rodent newborns are naked, so that in fact only the older juveniles
and adults of naked mole-rats have diverged in this regard from other rodents.
The hairlessness of non-newborns in naked mole-rats and humans is also simi-
lar in that in neither case is there either a dramatically thickened skin or armor
(although relatively more in naked mole-rats); it differs, of course, in that adult
humans have retained abundant hair on the head, in the pelvic region, and in the
armpits. The nudity of non-newborns in these two species, representing two of
seven or more independent origins of relative hairlessness, seems more reminis-
cent of the kind of hairlessness of newborn altricial mammals; these two species
may also be the only mammals in which nudity in newborns (probably) preceded
nudity in older juveniles and adults.
Hairlessness in newborns is widespread in mammals, as is absence or near
absence of feathers in newly hatched birds (see discussion of altriciality above).
This is probably the reason hairlessness has been regarded as part of a neotenic
trend, which may be a correct view in terms of developmental processes but does
not provide an explanation in evolutionary or selective terms. Phenomena such
as neoteny and allometry may represent inertial or constraining forces, in the
sense that natural selection must always operate on “last year’s model,” but in the
same sense all genetic, developmental, physiological, and morphological attributes
of organisms represent inertial elements for selection. Unless one assumes that
natural selection is helpless in the face of such inertias, the search for evolution-
ary (selective) explanations continues in approximately the same fashion as in
the absence of information about such inertias. The general assumption of such
searches is that selection is the principal (not the sole) guiding force of evolution.
Hairlessness and Ectothermy.—Newborn mammals that are both naked and
sometimes left by the mother in a nest also tend to be ectothermic, as do altricial
vertebrates in general, and this implies that there is merit in attempting to relate
the evolution of hairlessness to that of altriciality (see also Case, 1978). The human
baby is not ectothermic, but it is often said to be unusually capable of surviving
periods of lowered body temperature, and this feature may not be entirely inde-
pendent of its extreme altriciality. An ectothermic organism is one that relies for
its body temperature largely or entirely on external sources. Such organisms are
often described as having “poor” or “inadequate” means of thermoregulation. This
view is not productive of hypotheses as to the origin and basis of the trait, unless
one imagines, again, that selection has somehow been ineffective and a trait that
is disadvantageous has evolved. Such traits do evolve, as in senescence (Williams,
1957), but only under special conditions such as pleiotropy, with beneficial and
deleterious gene effects continuing in concert whenever they derive from the
same indivisible chunk of genetic material. Such deleterious traits are saved only
 Human Childhood } 193

because their inevitable companion traits are sufficiently beneficial to overcome

the deleterious effects and no way of divorcing the two effects has yet appeared.
In no organism, apparently, has a reason been generated for regarding ectothermy
as a deleterious pleiotropic effect, and, contrary to the situation with senescence,
no circumstances seem to exist that make such an explanation likely. Accordingly,
it seems parsimonious to assume that ectothermy evolved in altricial juveniles
and naked mole-rats because it is somehow directly advantageous, or because it
allowed some other change that was advantageous.
One correlate of ectothermy is a rather low metabolic rate, and it has some-
times been assumed that this is the source of the advantage (reviewed by Case,
1978). A lowered metabolic rate, for example, might allow naked mole-rats to sub-
sist on fewer calories and therefore suggests a continuing problem in caloric intake
that is greater or of a different nature than that encountered by the usual homeo-
thermic mammal.
A potentially profitable way to start thinking about the evolution of ectothermy
in a previously homeothermic animal is to consider that it has evidently become
more efficient, for whatever reason, for that animal to rely upon an external source
of warmth. This situation would seem to prevail whenever such external sources
are so reliable and effective that the expense of homeothermic machinery is
superfluous. To understand when such conditions might exist, one must consider
not only the external source of heat itself, but also the nature of threats, such as
inability to obtain food when it is crucial and inability to escape from predators
that are able to maintain a high rate of metabolism and predatory ability when
external heat sources are minimal or absent. Naked mole-rats, preyed upon largely
by snakes in their burrows (Sherman et al., 1991), have apparently been largely
relieved of homeothermic predators, and their tropical burrow systems are rela-
tively stable in both temperature and humidity.
Hairlessness and Altriciality.—Altricial juveniles that have given over virtually
all protection from predators and supplying of food to their parents (as with naked,
ectothermic forms) are in a position to retreat from homeothermy and use their
parents as the (primary) external heat source. Such a juvenile might gain from
refraining from use of nutrition provided by the parent to maintain a high meta-
bolic rate when the parent is absent, and instead conserve ingested calories for
later growth by maintaining a high metabolic rate only when external heat (par-
ent, sun) is available. In this fashion parents become suppliers of calories through
not only food itself, but also through providing heat for metabolism. This set of
attributes correlates with both nakedness in the juvenile and nakedness in at least
the part of the anatomy of the parent that most emphatically contacts the juvenile
during brooding (brood patches of birds, naked bellies and mammary glands of
mammals). It is probably significant that most naked juvenile birds and mammals
occur in litters, and single offspring are rarely naked. Nakedness allows extremely
rapid absorption of heat from extrinsic sources such as the sun, bodies of other
individuals, and warmed soil on sunny days and into the night. Coincidentally, it
194 { Human Social Evolution

also causes or allows rapid heat loss to other individuals, which are always close
relatives in the case of parental birds or mammals or colony members in naked
mole-rats.
Discussion.—These comparative arguments provide a background for thinking
about hairlessness, altriciality, and tendencies to be ectothermic in juvenile mam-
mals and birds, including the human baby. They leave unanswered, however, as
I suggested would be the case, precisely why older juvenile and adult humans are
relatively hairless. They also fail to answer in a satisfying way the questions why
the human baby is (1) apparently the only singly produced mammalian or bird
offspring that is naked, and (2) the only nonmarsupial mammalian offspring that
is both highly altricial and carried by the parents (newborns of apes are more altri-
cial than those of other primates, but much less so than the human baby: Dienske,
1986; some bat neonates are carried by the mother: Walker, 1975), as opposed to
being hidden and left, as with altricial rodent newborns and songbird hatchlings.

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9}

Indirect Reciprocity

Reverse Reciprocity
One day at the urinal
He chanced to drop a dollar bill.
It wafted down, he sees it yet,
Lying where the floor is wet,
One end doubtful, the other dry,
At first he thought he’d pass it by.
But then some lowly cunning won,
He folded it and passed it on.
And now a doubt forever lingers
For every dollar bill he fingers.
Alexander, 2011, p. 226
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 INTRODUCTION

The Basis of Morality, Richard Alexander on Indirect Reciprocity

Karl Sigmund

In Richard Alexander’s The Biology of Moral Systems (Alexander 1987; hereafter

BMS), the concept of indirect reciprocity plays a starring role. The author states
(p. 77) that “moral systems are systems of indirect reciprocity,” and writes (p. 95)
that “systems of indirect reciprocity become automatically what I am here calling
moral systems.” One chapter of the book is entitled “Moral systems as systems of
reciprocity” (p. 93). In this context, Alexander views “moral systems” as guides of
actions, or standards of conduct, and carefully separates them from the concept of
“morality,” which seems much harder to pin down.
When defining indirect reciprocity, Alexander contrasts it with the simpler
concept of direct reciprocity. The latter occurs when the return from the social
investment in another individual is expected from the actual recipient of the
beneficence. . . . “In indirect reciprocity, the return is expected from someone other
than the recipient of the beneficence. The return can come from essentially any
individual or collection of individuals in the group” (p. 85). The concept of indi-
rect reciprocity is also defined in Darwinism and Human Affairs (1979), where
Alexander writes:

Reciprocity can be divided into two types. Direct reciprocity occurs when
rewards come from the actual recipient of beneficence. Indirect reciprocity,
on the other hand, is represented by rewards from society at large, or from
others than the actual recipient of beneficence. We engage in both kinds
more or less continuously. (p. 49)

At the time when Alexander wrote these lines, in the late seventies, evolutionary
biology was just beginning to acknowledge the importance of direct reciprocity.
In particular, Robert Axelrod and William D. Hamilton were using computers to
conduct their famous round-robin tournaments of iterated Prisoner’s Dilemma
games, and to analyze the merits of Tit for Tat, the epitome of reciprocation
(Axelrod and Hamilton 1981, see also Axelrod 1984 and Hamilton 1996). The
simplest version of a Prisoner’s Dilemma game is obtained if two players can
independently decide whether or not to confer a benefit b to their co-player, at
200 { Human Social Evolution

cost c to themselves, with 0 < c < b. The dominating strategy here is to defect,
as this maximizes a player’s payoff, no matter what the other player does. But
if the game is repeated sufficiently often between the same two players, uncon-
ditional defection is not a good strategy against a Tit for Tat player, that is, a
player who confers a benefit to the co-player in the first round and from then
on does whatever the co-player did in the previous round. In particular, Axelrod
and Hamilton found that in various computer simulations of repeated Prisoner’s
Dilemma games, selection led to the emergence of Tit for Tat, and hence to the
evolution of cooperation. The work of Axelrod and Hamilton thus confirmed
Robert Triver’s seminal work (Trivers 1971), which had established reciprocity
as the second pillar, next to kin selection, to support altruism in evolutionary
biology. In the second edition of Richard Dawkins’s The Selfish Gene, a chap-
ter was added to celebrate the triumph of Tit for Tat: “Nice guys finish first”
(Dawkins 1989).
Indirect reciprocity is considerably more subtle than direct reciprocity. The
latter is based on the principle “I’ll scratch your back if you scratch mine,”
whereas the former is based on “I’ll scratch your back if you scratch someone
else’s” (Binmore 1994). The merits of this maxim seem more difficult to grasp.
They certainly require some sophistication. In Alexander’s words, “indirect reci-
procity involves reputation and status, and results in everyone in a social group
continually being assessed and reassessed by interactants, past and potential, on
the basis of their interactions with others” (BMS p. 85). In another statement,
“indirect reciprocity develops because interactions are repeated, or flow among
a society’s members, and because information about subsequent interactions can
be gleaned from observing the reciprocal interactions of others” (BMS p. 77). It
is this assessment of the actions of others (even if they are not directed at one-
self) which is the basis of moral judgements. It was Richard Alexander who first
emphasized the close connection between moral systems and reciprocity, in
stressing that systems of reciprocity need not be restricted to dyads of repeatedly
interacting individuals.
Every idea has its forerunners, and Alexander points out repeatedly that others
before him have dealt with generalizations of reciprocity, which he views as “the
binding cement of human social life” (BMS p. 111). Alexander was particularly
influenced by Trivers (1971, cf. Trivers 1986 and Trivers 2006). Darwin had also
anticipated the idea that assessments by others play a fundamental role in human
cooperation. In the Descent of Man, Darwin (1871) wrote that (in contrast to other
social animals such as bees or ants), “man’s motive to give aid no longer consists
solely of a blind instinctive impulse, but is largely influenced by the praise and
blame of his fellow men.“ We are all acutely concerned with how we are judged by
those around us.
Alexander thus squarely embraced the “misanthropic” tradition of many think-
ers before him, who suspected that costly and seemingly altruistic acts often pay,
in the long run, and therefore are not altruistic, even if actors themselves may
 Indirect Reciprocity } 201

think so. Their reward, or return, can come from various sources, either individu-
als, or collections of individuals, or even ‘society at large’. Let us look at these alter-
natives in turn.

FROM DIRECT TO INDIRECT RECIPROCITY

Let us suppose first that the return is provided by individuals. In direct reciprocity,
A helps B and B helps A. This yields a net benefit for both. For indirect reciprocity,
Alexander mentions two mechanisms by way of example (BMS p. 81). One is of the
form A helps B, B helps C, C helps A. Such cycles of helping were analyzed by Boyd
and Richerson (1989), who found, however, that they were fragile and unlikely to
occur, essentially because the “return” is so roundabout that the cycle can easily be
broken. The other mechanism suggested by Alexander was the following: A helps
B; C, observing, later helps A; A helps C. This means that A was rightly judged to
be a reliable partner by C, who uses this information to engage with A in direct
reciprocity. In this sense, indirect reciprocity acts as a kind of foreplay for direct
reciprocity. The corresponding strategy for the repeated Prisoner’s Dilemma was
termed Observer Tit for Tat (Pollock and Dugatkin 1992): it only deviates from Tit
for Tat in the first round, by refusing to help if the co-player, in the last interaction
with some third party, has refused to help.
But actually, the system proposed by Alexander works even if direct reciproc-
ity is explicitly excluded. This was shown by a series of models which assumed
that no players would ever meet the same co-player again. The principle is: “A
helps B; C, observing, later helps A,” which is just as before, except that the appen-
dix “A helps C,” which presumes a second meeting between A and C, is omitted.
The continuation in the modified version is implicit: “D, observing, later helps
C,” and so on.
It is worthwhile to explore the simplest models of this type (Nowak and
Sigmund 1998a, b; Lotem et al. 1999; Nowak and Sigmund, 2005; Pacheco et al.,
2006; Sigmund 2010). Thus, suppose that in a large population two players A and
B meet randomly, and each can either provide some help to the other or refuse to
help. (In an equivalent version, one player is randomly assigned the role of poten-
tial donor of the help, and the other the role of recipient.) If the same two players
never meet again, then Tit for Tat strategy makes no sense. But a closely related
variant of discriminating cooperation does. Players using this “reciprocating”
strategy refuse to help those players who have previously refused to help someone
else. In this way, beneficence is channeled toward those players who themselves
engage in beneficence. If C observes that A helps B, then C will help A, even if this
does not lead to repeated interactions between A and C. In a sense, this is a vicari-
ous return: C returns the help in B’s stead.
This model can be made more explicit in various ways. The conditional strategy
clearly requires that players have some information about the past behavior of their
co-players. Such information can be incomplete, and still lead to cooperation. It is
202 { Human Social Evolution

enough, for instance, to require that (a) with a certain probability q, the potential
donor knows whether the potential recipient has refused to help on some previ-
ous occasion, and (b) in the absence of information, the donor is willing to use
the “benefit of doubt”. If the probability q is larger than the cost-to-benefit ratio
c/b, cooperation can be sustained in the population: exploiters who never provide
help will rarely receive help, and do less well than the discriminating co-operators.
Even in this simple toy-model, it is of paramount importance that players can
acquire sufficient information about other group members. Clearly, such “social
scrutinizing” (to use Alexander’s term) is facilitated if individuals have a good
memory, and spend much of their time together. But it is likely that direct obser-
vation is not enough. In all human groupings, individuals exchange information,
and communicate what they observe through gossip. Here, the unique language
abilities of our species come into play. (“For direct reciprocity, you need a face;
for indirect reciprocity, you need a name.”[ Haigh, personal communication],
ca. 2005). Conversely, the need to exchange information about others may have
been a strong, possibly even the major, selective force behind the emergence of the
human language instinct (Dunbar 1996).
Both the ability to learn a language and the ability to learn a moral code seem
restricted to the human species. Alexander does “not exclude the possibility that
indirect reciprocity . . . will eventually be documented in some primates, social
canines, felines, cetaceans and some others” (BMS p. 85). Only few instances of
indirect reciprocation have been documented in nonhuman species so far (Bshary
and Grutter 2006, Rutte and Taborsky 2007). On the other hand, a large number
of economic experiments have shown that humans are highly prone to engage in
indirect reciprocity, and that (a) players known to help others usually increase
their chances in getting helped by third parties and (b) conversely the propensity
to help frequently more than doubles if players know that their decision will be
communicated. Help, in this context, is not an altruistic act, but an investment
into the social capital of reputation (Wedekind and Milinski 2000, Wedekind and
Braithwaite 2001, Seinen and Schram 2001, Milinski et al. 2001). This confirms
Alexander’s view that morality based on indirect reciprocity may be seen as self-
serving, because it causes a sufficient number of persons to regard the actor as a
good object of social investment (BMS p. 109).
The moral assessment of other group members can be captured, in its simplest
form, by labeling them “good” or “bad,” depending on whether they helped or
not. Clearly, such a binary assessment leads to a picture in black and white which
is much cruder than what we are used to in real life, but it suffices for a proof of
principle. Moreover, it raises an intriguing issue. In the most rudimentary form
of indirect reciprocity, the discriminating strategy, a cousin of Tit for Tat, extends
help to those who are “good” and refuses help to those who are “bad.” However,
a discriminating player who refuses to help a “bad” player becomes “bad” in the
eyes of all observers, and therefore less likely to be helped in turn. In order to
maximize the help one receives from discriminators, it would be better to never
 Indirect Reciprocity } 203

refuse to help, and thus to stop discriminating. But in a group without discrimina-
tors, exploiters go unpunished, and will spread. Cooperation cannot be sustained
in the long run.
A remedy coming immediately to mind is to assume that a refusal to help can
be justified, if it is directed toward a recipient with a “bad” image (Nowak and
Sigmund 1998a, Leimar and Hammerstein 2001, Panchanathan and Boyd 2003).
Such a justified refusal ought therefore not to be labeled as “bad.” This requires,
however, that observers are aware of the reputation of the potential recipient. This,
in turn, may require knowing the reputation of the recipient’s previous recipient,
and so on. It is questionable whether under normal conditions individuals have
enough information about their group members, or are sufficiently proficient at
coping with this information (Milinski et al. 2001). Moreover, we still have not
described the assessment system completely. While it obviously should be good
to refuse help to a “bad” player, it seems less clear whether giving help to a “bad”
player should be considered as good or bad, for example.
These considerations lead us to consider assessment systems which are not only
based on whether help is given or not, but also on the reputations of recipient
and donor. There are no less than 22×2×2 = 256 of them, even under the absurdly
oversimplified assumption that a player can only be “good” or “bad,” without inter-
mediate grades (Ohtsuki and Iwasa 2004, Brandt and Sigmund 2004). It turns out
that only 8 of them are stable, in the sense that a population which adopts them
will cooperate and cannot be invaded by unconditional strategies of always giv-
ing or always refusing help (Ohtsuki and Iwasa 2006). The competition of these
rudimentary “moral systems” under conditions which include the possibility
of occasional errors in action or judgement turns out to be remarkably difficult
to analyze (Ohtsuki and Iwasa 2007, Uchida and Sigmund 2010, Sigmund 2010,
Uchida 2010). Indeed, the status of a given group member will in general be differ-
ent for observers using different assessment rules. If additionally, the assessment
of a player is based on several actions of that player, or if there are more than two
labels for a player’s reputation (for instance, “good,” “bad,” and “indifferent”), the
complexity of the moral system explodes. Formalizing ethics appears to be harder
than formalizing logic. Practical philosophy defies mathematizing.
It is doubtful whether Alexander would view the investigation of formalized
systems of moral assessment rules as useful or relevant for evolutionary biology,
except as a means for quantifying verbal arguments. The delimitations required
for these models risk throwing out the baby with the bathwater. Indeed, models
of indirect reciprocity which isolate it from direct reciprocity on the one hand,
and from group interactions on the other, are artificial devices, useful for thought
experiments but far removed from reality. Alexander is more interested in the
fluid, and ever-growing boundaries of systems of reciprocity, and the effect of
this development on the human psyche. He suggests that “indirect reciprocity led
to the evolution of ever keener abilities to observe and interpret situations with
moral overtones” (BMS p. 100). “I regard indirect reciprocity as a consequence
204 { Human Social Evolution

of direct reciprocity occurring in the presence of interested audiences—groups

of individuals who continually evaluate the members of their society as possible
future interactants from whom they would like to gain more than they lose” (BMS
p. 93). In particular, “we use motivation and honesty in one circumstance to pre-
dict actions in others. . . . Humans tend to decide that a person is either moral or
not, as opposed to being moral in one context and immoral in another” (BMS
p. 94). And indeed, it is remarkable that ancient philosophers saw virtue as the
attribute of a person, whereas contemporary philosophers speak of virtue as the
attribute of an act, or a decision.
In most of Alexander’s descriptions of indirect reciprocity, the role of repu-
tation, and in particular the image of the potential recipients, is of central
importance. However, there seem to exist mechanisms of indirect reciprocity
which are not based on reputation. For instance, we could consider a situation
where first A helps B, and then B helps a third party C. There are many examples
of this. If someone holds the door open for us, we are likely to hold the door open
for the next. This type of indirect reciprocity, where the recipient returns the help,
but not to the actual donor, has also been observed in economic experiments and
seems less easy to explain theoretically.
Moreover, negative interactions may also be reciprocated. Alexander usually
speaks of “rewards” being returned, but retaliation clearly is also a widespread
form of reciprocation, and he mentions it, for instance in a table describing vari-
ous forms of indirect reciprocity (BMS p. 86), or by stating that “systems of indi-
rect reciprocity involve promises of punishment as well as reward” (BMS p. 96). In
the last two decades, experimental economists have uncovered a widespread pro-
pensity to punish those who are perceived as cheaters. So-called peer-punishment
is very effective at promoting cooperation (Fehr and Gächter 2002). Interestingly,
many individuals are ready to incur personal costs to punish norm breakers, even
if they themselves were not affected by the misdeameanour, but merely observed
it. This is certainly also a form of indirect reciprocity.

INDIRECT RECIPROCITY AND GROUP COMPETITION

So far, we have considered reciprocity based on returns by individuals. Alexander

stressed on several occasions that such a return could also be provided by collections
of individuals, as when he writes “indirect reciprocity, whereby society as a whole or
a large part of it provides the reward for the beneficence” (BMS p. 105). Societies pro-
vide not only rewards for beneficence, but also punishment for free-riding. In fact,
most punishment is not meted out by irate individuals in the form of peer-punish-
ment, but rather by institutions (Ostrom 1990; Yamagishi 1986; Sigmund et al. 2010).
Institutions can be viewed as tools enabling communities to provide positive or neg-
ative incentives. There is a striking similarity between institutionalized punishment
of free-riding and the repression of competition encountered in many examples of
cooperative groupings encountered in biological evolution (Frank, 1995).
 Indirect Reciprocity } 205

In a particularly interesting aside on indirect reciprocity, Alexander men-

tions that the reward which an individual obtains for acts of beneficence can
simply consist of increased success for the group (BMS p. 94). This observation
relates to an aspect which is crucial for the role played by moral systems, in
Alexander’s view.
Indeed, following Keith (1947), who stressed the competition between groups
as a main factor shaping human evolution, Alexander sees “morality as a within-
group cooperativeness in the context of between-group competition” (BMS p. 153).
According to his celebrated “balance of power” argument, the often lethal com-
petition between families, bands, tribes, and nation was the chief selective force
shaping human evolution. “In no other species do social groups have as their main
jeopardy other social groups of the same species” (BMS p. 77).
Alexander accordingly writes (BMS p. 194) that “indirect reciprocity is more
complex than is usually realized partly because of long-term benefits from being
viewed as an altruist, and partly because one must take into account benefits to
the individual that accrue from the success of his group in competition with other
groups.” This latter aspect is not, in general, associated with “indirect reciprocity”
nowadays. The former aspect has monopolized the meaning. The “long-term ben-
efits for being viewed as an altruist” help to establish generalized exchange systems
working to mutual advantage, even in the absence of strife between groups.
The role of group selection has been hotly debated by evolutionary biologists
during the last half-century. Mathematical models often use alternative expres-
sions, such as kin selection, or multi-level selection, sometimes with the intention
of avoiding semantic quarrels, and usually with the result of exacerbating them.
But there seems no reason to avoid the name “group selection” when one speaks of
groups fighting and annihilating each other. Individuals have to balance, in such
contests, their well-being within the group with the well-being of their group.
This viewpoint was shared by Darwin, who wrote: “There can be no doubt that
a tribe including many members who . . . were always ready to give aid to each
other and to sacrifice themselves for the common good, would be victorious over
most other tribes; and this would be natural selection” (p. 166). He did not say:
“and this is group selection,” but he obviously was aware of the tension between
individual and group selection when he wrote “He who was ready to sacrifice his
life . . . would often leave no offspring to inherit his noble nature. Therefore it seems
scarcely possible (bearing in mind that we are not here speaking of one tribe being
victorious over another) that the number of men gifted with such virtues could be
increased through natural selection” (page 163). The term in parentheses clearly
indicates that Darwin saw no way of explaining the evolution of such self-sacri-
ficing traits other than by violent intergroup conflict. In another passage, Darwin
stressed that “extinction follows chiefly from the competition of tribe with tribe,
and race with race” (page 186). To many ears, today, this sounds politically incor-
rect. But Darwin was very conscious of this dark side to human nature. Some
of the most remarkable examples of human cooperation occur in war, and other
206 { Human Social Evolution

forms of lethal conflict between groups, and it is well-known that day-to-day

solidarity dramatically increases in societies threatened from the outside.
That group selection can favor the emergence of cooperative traits has been
shown in countless models. It is all the more remarkable that the models and
experiments on indirect reciprocity which have been mentioned so far assume a
single, well-mixed population. They show that indirect reciprocity can work even
if the population is not structured into competing groups. Individuals who deviate
from the cooperative norm will have, on average, their long-term payoff reduced,
and thus are unlikely to be copied by others. This confirms Alexander’s view that
it is fallacious to assume that morality inevitably involves some self-sacrifice (BMS
p. 161). However, it confirms it in a setup which is different from Alexander’s.
A final remark: Economists have also been investigating extensions of the con-
cept of reciprocity, in parallel to evolutionary biologists. Their point of departure
was usually the so-called folk theorem on repeated games, which states that if the
probability of another round between the same two players is sufficiently high,
cooperation can be sustained by so-called trigger strategies, of which Tit for Tat is
but one example. A rational player would forgo the exploitation of a co-player in one
round if this jeopardizes collaboration in all future rounds. It is clear that if players
interact only once, a cheater cannot be held to account by its victim, and therefore
personal enforcement must be replaced by community enforcement. Game theo-
rists have shown that even if information is transmitted only imperfectly, coopera-
tion can be sustained, based on trigger strategies adopted by the whole community.
No rational player has an interest in deviating unilaterally (Rosenthal 1979, Sugden
1986, Kandori 1992, Ellison 1994, Okuno-Fujiwara and Postlewaite 1995, Bolton
et al. 2004a). The interest of economists in indirect reciprocity has been singularly
heightened in recent years by the fact that one-shot interactions between anony-
mous partners become increasingly frequent in today’s society. Web-based auctions
and other forms of e-commerce occur between strangers who never meet face-to-
face. They are built on rudimentary reputation mechanisms similar to those which
were developed in the simplest formal models capturing Richard Alexander’s ideas
on indirect reciprocity (Bolton et al. 2004b, Keser 2002).
Richard Alexander recognized indirect reciprocity based on reputation and
status as major factor in the emergence of moral systems in human societies. It
is amazing that the same simple, robust mechanisms that shaped early hominid
societies now play a central role in shaping the internet civilisation.

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 CLASSIFYING HUMAN EFFORT

The “Atoms” of Sociality

Excerpt from Alexander, R.D. 1986. The Biology of Moral Systems. New York,
Aldine Press.
If ethical, moral, and legal systems are ultimately understandable in evolution-
ary terms, then we ought to be able to explain them eventually, at even the most
complex and synthetic levels, by beginning with the “atoms” of sociality proposed
out of the life history and effort theories of modern evolutionary biology (see
table 9.1). We can note, first, that lifetimes are divisible into somatic and repro-
ductive effort, and, second, that reproductive effort can be subdivided, at least
in humans, into mating effort (on behalf of gametes), parental effort (on behalf
of offspring), and extraparental nepotistic effort (on behalf of collateral or non-
descendant relatives and descendants other than offspring). Next it is useful to
emphasize that humans are unusual among organisms in that all of their life effort
that is social in nature is permeated with reciprocity. The possibility of mutually
beneficial reciprocal interactions can cause both somatic and reproductive effort
to be socially mediated (nepotism, for example, can involve reciprocity in which
the return benefit goes to a relative of the originally beneficent individual). In turn,
reciprocity itself can be direct (A helps B, B helps A) or indirect (A helps B, B helps
C, C helps A. Or A helps B; C, observing, later helps A; A helps C). Reciprocity
is probably never complete, or balanced. (For further explanation, see below and
fig. 9.1; tables 9.1–9.5.) The effects of reciprocity and other forms of social media-
tion (competition, pseudoreciprocity) multiply the number of different “atoms” of
sociality that must be elucidated if a biological approach to human social behavior
is to be integrated with the approaches of philosophers and social and political
scientists.
1. Direct Somatic Effort. In this category of phenotypically selfish behavior are
included those aspects of somatic effort (i.e., directed toward growth, develop-
ment, and maintenance of one’s own phenotype or soma) that explicitly do not
involve benefits routed through other individuals. Direct somatic effort is medi-
ated by neither nepotism nor reciprocity. Examples are eating, drinking, seeking
shelter, and avoiding danger, when these actions are carried out without the assis-
tance or positive intervention of others. This category of behavior, which probably
corresponds most closely to the moral philosophers’ egoism (particularly when
the latter specifically involves seeking to promote one’s own welfare rather than
210 { Human Social Evolution

table 9.1 } Kinds of Effort and Their Outcomes1

“Atoms” of Sociality Kinds of Effort Phenotypically Genotypically
I. Somatic Effort Selfish Selfish
A. Direct
1. 1. Immediate payback
2. 2. Delayed payback
B. Indirect
3. Via indirect reciprocity
3. a. Immediate payback
4. b. Delayed payback
4. Via indirect reciprocity
5. a. Immediate payback
6. b. Delayed payback
II. Reproductive effort Altruistic Selfish
A. Mating effort
7. 1. Directly nepotistic (no social
mediation)
2. Indirectly nepotistic (social
mediation)
a. Via direct reciprocity
8. (1) Immediate payback
9. (2) Delayed payback
b. Via indirect reciprocity
10. (1) Immediate payback
11. (2) Delayed payback
B. Parental effort
12. 1. Directly nepotistic (no social
mediation)
2. Indirectly nepotistic (social
mediation)
a. Via direct reciprocity
13. (1) Immediate payback
14. (2) Delayed payback
b. Via indirect reciprocity
15. (1) Immediate payback
16. 1. Directly nepotistic (no social
mediation)
(2) Delayed payback
17. C. Extraparental effort
2. Indirectly nepotistic (social
mediation)
a. Via direct reciprocity
18. (1) Immediate payback
19. (2) Delayed payback
b. Via indirect reciprocity
Continued
 Indirect Reciprocity } 211

table 9.1 } Continued

“Atoms” of Sociality Kinds of Effort Phenotypically Genotypically
20. (1) Immediate payback
21. (2) Delayed payback
1
Direct somatic effort refers to self-help that involves no other persons. Indirect somatic effort involves reciprocity, which may
be direct or indirect. Returns from direct or indirect reciprocity may be immediate or delayed. Reciprocity can be indirect for two
different reasons, or in two different ways. First, returns (payment) for a social investment (positive or negative) can come from
someone other than the recipient of the investment, and second, returns can go either to the original investor or to a relative or
friend of the original investor.

someone else’s), is not as common as might be thought in today’s specialized social

environment. We can actually do very little for ourselves without some kind of
assistance, however indirect, by others.
2. Indirect (Socially Mediated) Somatic Effort. This kind of phenotypically
selfish behavior is routed through other individuals. Thus it may involve social
investments (initial costs, beneficent acts) in direct and indirect reciprocity. These
investments are expected eventually to be repaid to one’s self (as opposed to one’s
relatives, which would identify them as indirect nepotism). Examples are pur-
chases of goods to be used by one’s self (which may represent reciprocity in the
form of mutually beneficial exchanges of resources between buyer and seller) and
all social and other benefits given to others as investments in reciprocity when the
returns are realized through assistance to one’s self. There are two kinds of media-
tion of somatic effort: (a) direct assistance to Ego (i) by a relative (repayment to the
relative’s phenotype is likely not necessarily to be expected or required) and (ii) by
a nonrelative (eventual repayment is likely to be expected, to either the benevolent
individual or its relatives) and (b) assistance to Ego as a return on an investment
made by Ego as a part of somatic effort (i.e., direct reciprocity, such as, Ego helps
a nonrelative, expecting return assistance from the helped person at some later

table 9.2 } Indirect Reciprocity

Rewards (why altruism spreads)

1. A helps B
2. B helps A
3. C, observing, helps B, expecting that
4. B will also help (or overhelp) C
(ETC.)
Or
1. A helps B
2. B does not help A
3. C, observing, does not help B expecting that, if he does
4. B will not return the help
(ETC.)
212 { Human Social Evolution

Table 9.3 } Indirect Reciprocity

Punishment (why rules spread)

1. A hurts B
2. C, observing, punishes A, expecting that if he does not,
3. A will also hurt C
Or
4. Someone else, also observing, will hurt C, expecting no cost (ETC.)

date). We can predict that infants and very young children, especially, are evolved
to exhibit effort that elicits the (a) (i) kind of assistance above. What Trivers (1971)
called “reciprocal altruism” would include both the nepotistic and somatic (ego-
istic) effects of investments in both direct and indirect reciprocity (thus, while
beneficent, or initially costly, it would be only temporarily phenotypically altruistic
and not genetically altruistic or costly at all).
Although also egoistic in its consequences, socially mediated somatic effort
that involves initial costly investments (beneficence) may often be misinterpreted
as altruistic (that is, as genetically costly). Because of divisions of labor and social
interdependency in the modern world, this kind of egoism is also more common-
place than direct somatic effort.
3. Direct Nepotism. Included here are all investments in relatives for which the
return may be expected in genetic terms, through the reproduction of the assisted
relatives.
Mating effort is the most problematic form of effort placed here: it may be
viewed as selfish (hence, be confused with somatic effort), particularly in males,
who usually, as in mammals, strive to place their sperm inside the body of the
female, hence are in a better position to abandon the offspring to its mother’s care
than vice versa. A gamete, after all, is not an individual, and it possesses no genetic
materials other than those of its producer. But gametes are also not merely parts
of the phenotypes that produce them, and (except in species with haploid males)
are not genetically identical to their producers. Mating effort, moreover, is repro-
ductive effort that involves risks and expenditure of calories. Effort exerted on
behalf of gametes lowers the reproductive value of the individual as surely as that
exerted on behalf of offspring or other relatives. Perhaps the example is confusing

table 9.4 } Indirect Reciprocity

Deception (why cheating spreads)
1. A1 makes it look as though he helps B
2. C1 helps A1, expecting that A1 will also help him
3. C2 observes more keenly and detects A1’s cheating and does not help him (avoids or punishes him)
4. A2, better at cheating, fools C2
5. C3 detects A2’s cheating (ETC.)
C1 -> C2 -> C3; A1 -> A2 -> A3 Either learning or evolution (or both)
Table 9.5. Interactions of Motivations and Outcomes Determining Morality and Immorality of Social Actsa
Motivations
Doesn’t know or think about what he is doing Does these things deliberately
Outcomes of Social Acts Considered to be insane or Considered to Believes he is selfish and expects to Believes he Believes he is altruistic but expects to win despite
incompetent (i.e., can- be lazy or win because of selfishness is altruistic altruism
not know - includes thoughtless - and expects
non-humans does these things to win
without thinking because of Expects reward on Earth Expects reward in
(could know altruism Heaven
but doesn’t)

Sees his way of life Sees his life as a Sees his Satisfying Burden Satisfying Burden
as satisfying: acts burden (as com- way of life
this way because pared to other as either
he enjoys it lives possible) satisfying or
as a burden

Helps only self 1 2 3 4 5 6 7 8 9

Neutral (e.g. baby) Immoral Immoral Unlikely Immoral Immoral Unlikely Unlikely Unlikely
Helps only self and relatives 10 11 12 13 14 15 16 17 18
Neutral Immoral Immoral Unlikely Probb Probb Probb Probb Probb
Helps self, relatives, and friends who are likely to reciprocate 19 20 21 22 23 24 25 26 27
with interest Neutrald Immoral? Immoral Unlikely Probc Probc Probc Probc Probc
Helps self, relatives, reciprocating friends, and others in the 28 29 30 31 32 33 34 35 36
presence of potential reciprocators Neutrald Moral? Immoral Unlikely Probc Probc Probc Probc Probc
Helps all of the above, and also helps strangers when it is not 37 38 39 40 41 42 43 44 45
too costly, even when not in the presence of reciprocators Neutrald Moral Unlikely? Unlikely Moral Moral? Moral? Moral Moral
Helps anyone who needs it even if the 46 47 48 49 50 51 52 53 54Moral
immediate cost is great Neutrald Moral Unlikely Unlikely Moral Moral? Moral? Moral
Helps others indiscriminately while maintaining self at 55 56 57 58 59 60 61 62 63
approximately the lowest level Neutrald Moral Unlikely Unlikely Moral Moral? Moral? Moral Moral
consistent with doing this effectively (Saint) (Saint)
a
I have speculated as to how each category of act is likely to be judged. Problematic cases illustrate the difficulty of deciding questions of morality when self-interest is broadened to include reproductive (genetic) interests,
and when motivation comes to include realizations of the nature of such interests. Squares 25–32 and 41–48 would probably be marked “moral” by those unaware of biological considerations because they seem to involve
self-sacrifice. An evolutionary biologist might regard all squares as representing possible behaviors, and as all possibly representing self-interested behaviors, but he might also regard squares 55–63 as less likely than would
nonbiologists. Biologists would also be more likely to search for ways in which squares 55–63 could represent behaviors that serve the actor’s interests.
b
Behaviors that will probably be seen by most as immoral because of outcomes and despite motivations. Prob, problematic.
c
Behaviors that will probably be seen by most as moral because of outcome and motivation combined.
d
Desirable behavior even if morally neutral.
214 { Human Social Evolution

primarily because mating effort involves interactions of two individuals, and there
is a tendency to compare the relative “selfishness” of the two. Also, in mating effort,
as compared to other reproductive effort, the genetically selfish aspects of acts may
be relatively more apparent than their phenotypically altruistic aspects. We are
more likely to regard a male mammal’s effort to place his gametes in a warm, safe
place where they can fertilize an egg as an act of reproductive selfishness that ben-
efits him in relation to the female involved than we are to see it as an act of pheno-
typic altruism benefiting his gametes.
4. Indirect (Socially Mediated) Nepotism. This category of reproductive effort
includes investments in reciprocity in which returns from one’s beneficence may
reasonably be expected to be realized by relatives rather than one’s self (e.g., hero-
ism or good will created by one’s benevolent acts may cause benefits to accrue to
one’s family).
Although the last two categories of behavior are not easily understood as a part
of the moral philosophers’ category of “egoism,” neither are they either indiscrimi-
nately or genetically altruistic or utilitarian; if carried out appropriately in evolu-
tionary terms, all of the above four kinds of behavior are genetically selfish, even
those which are phenotypically self-sacrificing or (temporarily) altruistic (or benefi-
cent) (Alexander, 1974, 1979a).
5. Reciprocity (Direct and Indirect). It appears to me that all reciprocity so far
documented in nonhuman organisms is appropriately termed direct reciprocity, in
which the return from a social investment in another (i.e., an act of “temporary”
altruism) is expected from the actual recipient of the beneficence, although not
necessarily in the same currency (Trivers,1971; Axelrod, 1984). In indirect reciproc-
ity (Alexander 1977a, b, 1979a, 1982, 1985b), the return is expected from someone
other than the recipient of the beneficence (tables 9.2–9.4). This return may come
from essentially any individual or collection of individuals in the group. Indirect
reciprocity involves reputation and status, and results in everyone in a social group
continually being assessed and reassessed by the interactants, past and potential,
on the basis of their interactions with others. I do not exclude the possibility that
indirect reciprocity, in this sense, will eventually be documented in some pri-
mates—especially chimpanzees (e.g., de Waal, 1982, 1986) social canines, felines,
cetaceans, and some others.
What I am calling “indirect reciprocity” Trivers (1971) referred to as “general-
ized reciprocity.” I avoided the latter term because of the way Sahlins (1965) used
it—cf. Alexander (1975, 1979a, 1985). Sahlins typified generalized reciprocity as
involving one-way flows of benefits in which the expectation of return is vague or
nonexistent. He included nepotism, citing the case of a mother nursing her child,
and with respect to nonrelatives seemed to be referring to what we would now call
genetic or reproductive altruism. Perhaps both terms will survive: Indirect reci-
procity for cases in which the return explicitly comes from someone other than the
recipient of the original beneficence, and generalized reciprocity for social systems
in which indirect reciprocity has become complex and general.
 Indirect Reciprocity } 215

Reciprocity in nonhuman organisms (Trivers, 1971; Axelrod and Hamilton,

1981) may have arisen between bonded males and females in species with both
maternal and paternal care. In such cases it may have developed out of mating
effort (e.g., a male gives a gift to a female and is allowed to copulate), subsequently
as indirect nepotism through effects on offspring produced jointly by the pair (e.g.,
a female copulates with a male and he gives her a gift which she uses to rear his
offspring). Alternatively (and perhaps more likely), reciprocity may have arisen as
a modification of direct nepotism in which flows of benefits began to pass in both
directions successively rather than just one direction from one relative to another.
Benefits can be returned to a social investor as a part of the egoistic behavior of the
individual returning it—i.e., at no cost to that individual. In such instances, pos-
sibilities for cheating are essentially nonexistent and the overall complexity of the
mental activities accompanying evolution of the act will be reduced in comparison
to reciprocity per se. Connor (1986) calls such interactions “pseudoreciprocity.” In
terms of my examples, it would be pseudoreciprocity if the female receiving a gift
from a courting male copulated with him strictly because it was to her immediate
advantage. If the act was at least temporarily costly—e.g., if she was initiating a
longer-term exchange of beneficence—then the step into direct reciprocity would
have been taken. I agree with Connor that most discussions of “reciprocity” in
nonhuman species probably involve pseudoreciprocity instead.
It will be seen that subdividing somatic effort into direct and indirect—and
reproductive effort into mating effort, parental effort, and extraparental nepotis-
tic effort—creates five major “atoms” of sociality. The overlays of reciprocity and
pseudoreciprocity, with the possibility of immediate or delayed returns, brings
the number of such “atoms” to 21 (table 9.1). Further complicating the picture are
additional overlays involving consciousness and deliberateness in different kinds
of acts (table 9.5).
Identifying atoms or units of sociality for the purpose of understanding the flow
of human social interactions seems to be a matter of locating units or transactions
that can substitute for one another in the functioning of nepotism or reciprocity.
I mean to suggest units for which cost-benefit analyses can be accomplished more
or less independently, units that can be regarded as alternatives or options for the
purpose of compensating beneficence or cheating. I believe that without very large
numbers of such units, and large numbers of alternative players, reciprocity could
not become complex. Human sociality seems composed of countless such units,
and I think we are constantly separating the flow of our social interactions into
units (acts, interactions, transactions) that we can use for our own purposes (e.g.,
investments intended to test the readiness of another to repay social debts with
interest).
In light of the biological separation of lifetimes into somatic and repro-
ductive effort, it is curious that moral philosophers’ views of moral behavior
usually require either 100% selfishness or 100% altruism but scarcely ever com-
binations of the two; with a few exceptions (e.g., Whiteley, 1976; MacIntyre,
216 { Human Social Evolution

1981b), philosophers seem to find it impossible to combine the two. The reason
seems to be the view that consistency is required in moral behavior (i.e., to be
moral one must advocate for himself only those rights and privileges he will
advocate equally strongly for all others), and a dual human nature (i.e., involv-
ing both egoistic and altruistic tendencies or acts) has inconsistency built into
it. Whiteley (1976) and MacIntyre (1981b) believe it is possible to be consistently
(morally) egoistic, but I find it difficult to imagine that a true egoist would be
likely to advocate the right of others to resources that egoism would require
him to seek for himself. One has to presuppose that resource seeking does not
involve conflict and ignore the argument that success is relative. The only time
that utilitarianism (promoting the greatest good to the greatest number) is pre-
dicted by evolutionary theory is when the interests of the group (the “greatest
number”) and the individual coincide, and in such cases utilitarianism is not
really altruistic in either the biologists’ or the philosophers’ sense of the term.
It seems more likely that restraints on individuals and subgroups serving their
own interests occur solely because of the likelihood of prohibitive costs being
imposed by some part of the rest of society; this is precisely the definition of
moral systems I am developing here.
Moral philosophers have not treated the beneficence of humans as a part,
somehow, of their selfishness; yet, as Trivers (1971) suggested, the biologist’s view
of lifetimes leads directly to this argument. In other words, the normally expressed
beneficence, or altruism, of parenthood and nepotism and the temporary altru-
ism (or social investment) of reciprocity are expected to result in greater (genetic)
returns than their alternatives.
If biologists are correct, all that philosophers refer to as altruistic or utilitarian
behavior by individuals will actually represent either the temporary altruism (phe-
notypic beneficence or social investment) of indirect somatic effort or direct and
indirect nepotism. The exceptions are what might be called evolutionary mistakes
or accidents that result in unreciprocated or “genetic” altruism, deleterious to both
the phenotype and the genotype of the altruist; such mistakes can occur in all of
the above categories (see also Alexander, 1979a, table 1, for a discussion of genetic
and phenotypic altruism). Part of our analysis (p. 100ff.) will involve the effects of
certain kinds of indirect somatic effort and nepotistic altruism on the numbers
and significance of such accidents by others. The question involved is whether
or not we are evolved to promote such mistakes in others, and to resist them in
ourselves, and the effects of any such tendencies on the nature of our moral and
legal systems.

PHILOSOPHY AND CONFLICTS OF INTEREST

Among social and political scientists, moral philosophers, ethicists, and others
who study and think about moral questions, probably everyone would agree that
conflicts of interest, and the human attitudes, tendencies, and actions that derive
 Indirect Reciprocity } 217

from histories of conflicts of interest, are alone responsible for ethical, moral, and
legal questions. On the other hand, not everyone who writes in this arena headlines
his discussions with the question of conflicts of interests. I think of such recent
and influential volumes as John Rawls’ (1971) A Theory of Justice, Richard Brandt’s
(1979) A Theory of the Good and the Right, William Frankena’s (1973, 1980) Ethics
and Thinking About Morality, and Lawrence Kohlberg’s (1981) The Philosophy of
Moral Development. One cannot find general discussions of the nature of interests
or the quantification of their conflicts; or do phrases like “conflict of interest,” “dif-
ferences of opinion,” or even “disagreements” and “interests” appear in either the
tables of contents or the indexes. Similarly, if one keeps the question of conflicts
of interest, at both individual and various group levels, in mind while reading the
essays of Richards (1986b) and the responses to them, I believe some of the seem-
ingly most difficult questions are simplified.
The general theory of interest, called for by Pound (quoted pp. 33–34; see also
Pound, 1959) has not been developed, and is discussed by few other authors.
Although everyone who writes in this arena may recognize that disagreements
and conflicts about interests are what underlie moral systems, for some reason few
have been compelled to generalize about them or dwell on their bases.
It is my impression that many moral philosophers do not approach the problem
of morality and ethics as if it arose as an effort to resolve conflicts of interests. Their
involvement in conflicts of interest seems to come about obliquely through discus-
sions of individuals’ views with respect to moral behavior, or their proximate feel-
ings about morality—almost as if questions about conflicts of interest arise only
because we operate under moral systems, rather than vice versa.
An excellent example of a philosophical discussion that does not directly con-
front the question of whether the whole flow of social interactions depends on
conflicts and confluences of interest is that of Callahan (1985). Writing on “What
Do Children Owe Elderly Parents?” Callahan alludes to interests driving the inter-
action only twice. On p. 32 he notes “As a piece of practical advice, however, it
[honoring fathers and mothers] once made considerable sense. In most traditional
and agricultural societies, parents had considerable power over the lives of their
offspring. Children who did not honor their parents risked not only immediate
privation, but also the loss of the one inheritance [land] that would enable them
to raise and support their own families.” On p. 36, speaking of “The poor,” he com-
ments “ . . . adults with elderly parents ought not to be put in the position of trying
to balance the moral claims of their own children against those of their parents,
or jeopardizing their own old age in order to sustain their parents in their old age.
Though such conflicts may at times be unescapable, society ought to be struc-
tured in a way that minimizes them.” It is as if Callahan did not consciously con-
sider whether or not conflicts of interest were the central issue of the topic he was
discussing.
Most of Callahan’s article attempts to resolve the problem of care for the
elderly in contemporary society by wrestling from every possible direction with
218 { Human Social Evolution

proximate mechanisms, such as the feelings of children toward their parents, of

parents toward their children, and of “society” toward both. This exercise ends
inconclusively, as if presaged by his statement (p. 35). “I am searching here with
some difficulty for a way to characterize the ethical nature of the parent-child rela-
tionship, a relationship that appears almost but not quite self-evident in its recip-
rocal moral claims and yet oddly elusive also.”
The trouble is, there is no one “parent-child relationship” and the whole problem
of care for the aged has arisen, not so much because lives have been prolonged, but
because familial bonds have been fractured, explicitly in ways that have made con-
fluences of interest between aged parents and their children much less likely. Self-
interested reasons for children to care for aged parents have all but disappeared,
and I suggest that this is why their care is being thrust upon “society” and why
it has become so expensive. This expense to society is, in turn, why “society” has
become concerned to discuss the question of children’s moral and ethical obliga-
tions to their parents. I see no likelihood that such questions can ever be elucidated
by confining the arguments to proximate mechanisms. Callahan does conclude that
“A minimal duty of any government should be to do nothing to hinder, and if pos-
sible do something to protect, the natural moral and filial ties that give families
their power to nurture and Sustain.” He does not delve deeply into the basis for
this (or any other) “should,” however. Somehow he also realizes that “To exploit
that bond by coercively taxing families is, I believe, to threaten them with great
harm . . . It . . . presupposes a narrower form of moral obligation . . . than can natu-
rally be defended . . . [and] promises to rupture those more delicate moral bonds ...
that sustain parents and children in their lives together.” I think that what Callahan
is describing here are the probable repercussions of forcing children to care for
their parents, repercussions that will exacerbate the overall problem and cause even
greater expense to “society.” I am not suggesting that intensive analyses of the feel-
ings (and other proximate mechanisms) that underlie moral dilemmas are not use-
ful; I think it is obvious they are essential. I am, rather, saying that cases like the
relationships between parents and children in different societal milieus show that
the underlying conflicts of interest drive the proximate mechanisms, at least as sig-
nificantly as the reverse. To try to understand one without the other seems futile.
In contrast to Callahan’s discussion, Strong (1984) develops an excellent and
well-documented discussion of conflicts of interest among neonates, parents, and
physicians, which I believe shows well how thinking directly in terms of conflicts
and confluences of interest of the involved parties can lead to potentially satisfying
ways of making decisions. At one point (p. 15) he describes three useful reasons for
“ . . . The general principle that the patient comes first”:
One is the utilitarian consideration that people will be more likely to seek
health care if they trust doctors, and people are more likely to trust doc-
tors if it is generally perceived that doctors put the interests of patients
first. Another consideration is that a trusting relationship has therapeutic
 Indirect Reciprocity } 219

advantages in that it reduces anxiety and enhances compliance. In addi-

tion, because physicians in general are known to espouse the principle of
putting patients first, patients assume that doctors will act accordingly. As
Albert Jansen and Andrew Jameton see it, patients have a right to make that
assumption, and doctors are morally obligated not to disappoint them.
When patients are incompetent, society itself prudently (and rightfully)
requires physicians to put patients first, since any of us might some day
become incompetent patients. In addition, there may be an implied agree-
ment with the incompetent patient’s family to do what is best for the patient.
None of these considerations, however, seems to support the premise
that the infant comes first even if that means great sacrifice by the family.
The therapeutic advantage and the implicit agreement with the patient do
not apply in the case of newborn patients. Neither does the prudential rea-
son, since none of us will be neonates again. Besides, the utilitarian goal of
encouraging parents to seek medical care for their children would seem to
be served just as well, if not better, by the principle of putting the infant first,
unless doing so creates a great burden for the family. Furthermore, con-
cerning any implied agreement with an incompetent patient’s family, it is
doubtful that parents generally agree, either implicitly or explicitly, that the
physician is to do what is best for the infant regardless of the burden to par-
ents. I submit, then, that there is no basis for the view that the duty to the
patient is absolute in the kind of case we are considering.
There is one curious omission in Strong’s discussion: nowhere does he
acknowledge that physicians might have interests of their own that could conflict
with those of both parent and neonate, or most especially with those of parents
in the matter of “aggressive treatment” to save neonates: “Thus, when doctors
make unilateral judgments about newborns with the avowed or implicit pur-
pose of protecting the infant’s interests, they are not behaving paternalistically
toward anyone.” But separate interests on the part of the physician are an obvious
probability, and I suggest that the forcing apart of physicians’ and their patients’
interests by the impersonality and nonrepetitiveness of physician-patient inter-
actions in modern urban society is a principal reason for the rises in dissatis-
faction, litigation, and the expenses of medical care. For example, excessive use
of diagnostic procedures (that are often risky to the patient) are carried out to
protect the interests of physicians and hospitals because, I believe, physicians and
hospitals have lost the ability to convince patients that they have indeed assumed
the medical interests of the patient as if they were their own. Family doctors in
rural settings with stable populations of interrelated, interacting people suffered
far less from such difficulties, partly because their reputations were constantly
on the line. Patients had ways other than litigation to reciprocate inferior treat-
ment, and more reasons to believe they were obtaining the best care the physician
could give.
220 { Human Social Evolution

The closest Strong comes to acknowledging that physicians may have separate
interests of their own is the following:
There are vested interests, in that an entire medical subspecialty has devel-
oped to care for impaired newborns. Just try to suggest to neonatologists
and NICU nurses that their patients are not persons! (p. 14).
Contrary to most authors, a few who have dealt with moral issues have focused
quite directly on conflicts of interest. Thus, Perry (1954, pp. 87, 165) noted that:
It is an open secret . . . that morality takes conflict of interest as its point of
departure and harmony of interests as its ideal goal (p. 87).
The ultimate data of moral science are not men’s approbations and dis-
approbations, but conflicts of interest, and the organizations of interests by
which they are made non-conflicting and cooperative (p. 135).
The philosopher, Hans Kelsen (1957), is another example, and in his book What
Is Justice? he stated what is meant by conflicts of interests (pp. 2–4):

Where there is no conflict of interests, there is no need for justice. A conflict

of interest exists when one interest can be satisfied only at the expense of the
other; or what amounts to the same, when there is a conflict between two
values, and when it is not possible to realize both at the same time; when
the one can be realized only if the other is neglected; when it is necessary to
prefer the realization of the one to that of the other; to decide which one is
more important, or in other terms, to decide which is the higher value, and
finally; which is the highest value.

Despite this clear statement and the rather grand essay written 16 years earlier
by Roscoe Pound (see pp. 33–34), neither Kelsen nor any other author I have dis-
covered sets out to identify interests and quantify their conflicts and confluences
(although Strong, 1984, comes close); most do not even acknowledge this as a mat-
ter of importance. Piecemeal efforts are as old as history, but there seems to have
been no effort toward a general theory.
Why should it be true that the very disciplines preoccupied with conflicts of
interest should deal with them as if they were something other than the central issue?
Perhaps the authors involved would respond to this question by saying: “Rubbish!
Of course we know that conflicts of interests are the heart of the problem. The reason
we don’t dwell on them is because we know their role and importance so well.”
Perhaps. But precisely the same thing is sometimes said about altruism. At a
recent meeting at the University of Michigan, a prominent moral philosopher
said, in evident puzzlement, “We have been discussing altruism forever. What is
all the recent excitement from biology about?” The excitement exists because the-
ories of inclusive-fitness-maximizing (Hamilton, 1964) and reciprocity (Trivers,
1971) enable us to formulate testable hypotheses about aspects of altruism that
previously could not be investigated scientifically. A new understanding of what
human interests are all about might similarly justify a reexamination of the central
 Indirect Reciprocity } 221

question of conflicts of interest in connection with morality and ethics and the
general conduct of people. I think we have such a new understanding and, as with
our new understanding of altruism, it comes from biology. Grant (1985), for exam-
ple, remarks that “When Rawls speaks of human beings as rational, he means that
they are able to calculate their self-interest. . . . What men primarily calculate about
are those good things which lead to comfortable self-preservation.” It is a major
argument of this book that this prevalent view simply will not allow us to analyze
human sociality to the core. (A more extensive discussion of moral philosophy
occurs later on pp. 145ff.)

MORAL SYSTEMS AS SYSTEMS OF INDIRECT RECIPROCITY

The problem, in developing a theory of moral systems that is consistent with

evolutionary theory from biology, is in accounting for the altruism of moral
behavior in genetically selfish terms. I believe this can be done by interpreting
moral systems as systems of indirect reciprocity.
I regard indirect reciprocity as a consequence of direct reciprocity occurring in
the presence of interested audiences-groups of individuals who continually evalu-
ate the members of their society as possible future interactants from whom they
would like to gain more than they lose (this outcome, of course, can be mutual).
Returns from indirect reciprocity may take at least three major forms:
(1) the beneficent individual may later be engaged in profitable recipro-
cal interactions by individuals who have observed his behavior in directly
reciprocal interactions and judged him to be a potentially rewarding inter-
actant (his “reputation” or “status” is enhanced, to his ultimate benefit); (2)
the beneficent individual may be rewarded with direct compensation from
all or part of the group (such as with money or a medal or Social eleva-
tion as a hero) which, in turn, increases his likelihood of (and that of his
relatives) receiving additional perquisites; or (3) the beneficent individual
may be rewarded by simply having the success of the group within which he
behaved beneficently contribute to the success of his own descendants and
collateral relatives.
Obviously, various forms of punishment, including ostracism or social shun-
ning, can also be applied to individuals repeatedly observed not to reciprocate
adequately or follow whatever codes of conduct may exist.
Typically, then, in interactions solely involving direct reciprocity, individuals
may be expected to seek a net gain, although (1) this does not necessarily come at
the expense of the other interactant (i.e., both may profit) and (2) the net gain may
only be realized after a long iterated series of interactions, anyone or fraction of
which may actually yield a net loss for the individual in question. Even in directly
reciprocal interactions, however, net losses to self (and even explicitly greater losses
than those of the partner) may be the actual aim of one or even both individuals,
if they are being scrutinized by others who are likely to engage either individual
222 { Human Social Evolution

subsequently in reciprocity of greater significance than that occurring in the scru-

tinized acts. In effect, what goes on in such cases could be termed “social hustling,”
in which a “player” more or less deliberately (though conscious purpose is not a
requirement) loses in order to “set up” the observer for a later overcompensating
gain. I am referring to all effects of such social scrutinizing as indirect reciprocity.
If current views of evolutionary processes are correct, reciprocity flourishes when
the donated benefits are relatively inexpensive compared to the returns (Hamilton,
1964; Trivers, 1971; Alexander, 1974; West-Eberhard, 1975). This kind of gain is pos-
sible under two circumstances: the first is when threats or promises extrinsic to the
interactants cause joint similar efforts to be worth more than the sum of their sepa-
rate contributions, leading to more or less symmetrical cooperation. The second is
when the contributions of partners in reciprocity are different, leading to division
of labor. The second situation can arise out of different abilities or training in dif-
ferent contributors, or from differences in their accumulated resources. Systems of
indirect reciprocity as expressed in humans require memory, consistency across
time, the application of precedents, and persistent and widely communicated con-
cepts of right and wrong (Trivers, 1971, 1985; Alexander, 1977–1982; Axelrod and
Hamilton, 1981). They become, automatically, what I am here calling moral svstems.
I believe that the feeling that human behavior is out of reach of biological analyses
arises, not so much because we are confused by the existence of “culture” or socially
heritable learning (the reason usually given), but because culture includes systems
of indirect reciprocity (moral, ethical, and legal systems) by which the costs and
benefits of acts deemed by others to be socially positive or negative can be manipu-
lated. The “problem of culture,” then, may not be so much one of ontogenetic dis-
junction (as most authors seem to imply—meaning that at some point learning or
culture takes over and the human organism begins to operate independently of its
evolutionary heritage), but rather a failure to appreciate the pervasiveness and the
consequences of indirect reciprocity. Systems of indirect reciprocity, and therefore
moral systems, are social systems structured around the importance of status. The
concept of status implies that an individual’s privileges, or its access to resources,
are controlled in part by how others collectively think of him (hence, treat him)
as a result of past interactions (including observations of interactions with oth-
ers). Status can be determined by physical prowess, as in those nonhuman (animal)
dominance hierarchies in which coalitions are absent, or (as in humans) by mental
or social prowess. Mental and social prowess, in this sense, includes (as in moral
systems) effectiveness and reliability in reciprocity and cooperation.
Once social interactions become instrumental in establishing status, then testing
and practice, as in the forms typically called “play,” may become prominent. Play
represents practice for later status-affecting interactions, but it also affects current
and projected status. In humans, social-intellectual play in the form of humor has
become uniquely elaborate. This kind of play, moreover, unlike most forms of play,
is prominent across all of adult life. As with physical play in humans (Alexander,
1974), humor has also come to include unique group-against-group forms (i.e.,
“ostracizing” humor, such as ethnic and racial jokes) (Alexander, 1986b).
 Indirect Reciprocity } 223

WHERE DO RULES COME FROM

As soon as planning, anticipating, “expecting” organisms are interacting without
complete overlap (confluence) of interests, then each of two interactants may be
expected to include in (add to) its repertoire of social actions special efforts to
thwart (intercept, alter) the expectations of the others—explicitly in ways designed
to be costly to those others and beneficial to himself. Interruption of another’s
expectations will be costly to that other when the expectation involves some
investment (cost), or when pursuing it has been done in a way that is less costly
because it did not allow for the possibility of the kind of interruption that the first
party caused. I suggest, then, that the expense of investing in expectations, and the
possibility of doing so with less expense if certain kinds of interruptions are fore-
stalled, are the essential reasons for the invention and maintenance of rules. Rules
are aspects of indirect reciprocity beneficial to those who propose and perpetuate
them, not only because they force others to behave in ways explicitly beneficial
to the proposers and perpetuators but because they also make the future more
predictable so that plans can be carried out. This proposition is subtly, but signifi-
cantly, different from that implied by Rawls (1971, p. 6):
In the absence of a certain measure of agreement on what is just and unjust,
it is clearly more difficult for individuals to coordinate their plans efficiently
in order to ensure that mutually beneficial arrangements are maintained.
Distrust and resentment corrode the ties of civility, and suspicion and hos-
tility tempt men to act in ways they would otherwise avoid. So while the
distinctive role of conceptions of justice is to specify basic rights and duties
and to determine the appropriate distributive shares, the way in which a
conception does this is bound to affect the problems of efficiency, coordina-
tion, and stability.
The significance of indirect reciprocity has to do not only with rules, but with
intent (table 9.5), and the general levels of altruism prevailing in the society.
Because systems of indirect reciprocity involve promises of punishment as well
as reward they lead to avoidance of selfishness as well as positive acts of altruism.
This is why, I believe, humans tend to decide that a person is either moral or not, as
opposed to being moral in one time or context and immoral in another, and why
intent is said to be “nine-tenths of the law.” We use motivation and honesty in one
circumstance to predict actions in others.
Seeing morality as self-serving because of indirect reciprocity enables us to
visualize it in two stages or as involving two kinds of outcomes for acts widely
regarded as immoral:
1. If I do that (“immoral thing”) to someone I am apt to suffer costs greater
than the benefits, imposed on me by the other members my group as a
result of indirect reciprocity (within-group indirect reciprocity).
2. If I do that (“immoral thing”) to someone I will foster, or at least not
restrain, the development of a pattern of within-group behavior that will
224 { Human Social Evolution

eventually impose a cost on me greater than the benefits. These costs

will be imposed on me either by a change of rules that I precipitate or
promote against my long-term interests or by the ability of members of
groups other than my own to injure or destroy my group because of its
lack of unity (between-group indirect reciprocity). Awareness of this
later possibility by my group members will cause them to be even more
watchful of my behavior within the group, thus increasing the costs of
“immoral” actions monitored by within-group reciprocity.
The consequences of indirect reciprocity, then, include the concomitant spread
of altruism (as social investment genetically valuable to the altruist), rules, and
efforts to cheat (tables 9.2–9.4). I would not contend that we always carry out cost-
benefit analyses on these issues deliberately or consciously. I do, however, contend
that such analyses occur sometimes consciously, sometimes not, and that we are
evolved to be exceedingly accurate and quick at making them (table 9.5).

DISCRIMINATE AND INDISCRIMINATE BENEFICENCE

The beneficence involved in human nepotism and direct reciprocity is discrimi-
native: different relatives, and relatives of different needs, are distinguished.
Friends are treated individually. As yet, no organism outside clones has been
shown to display population-wide indiscriminate beneficence, and I will argue
that, with the exception of clones and certain kinds of eusociality (especially, in
termites, ants, wasps, and bees), or in human systems of indirect reciprocity does
a modicum of essentially indiscriminate beneficence or social investment exist in
large groups
Indirect reciprocity must have arisen out of the search for interactants and
situations by which to maximize returns from asymmetrical, hence highly prof-
itable direct social reciprocity. One consequence of large complex societies in
which reciprocity is the principal social cement and indirect reciprocity is preva-
lent is that opportunities for such mutually profitable asymmetrical reciprocal
interactions are vastly multiplied. This situation, in turn, fosters the appear-
ance of tendencies to engage indiscriminate social investment (or indiscriminate
beneficence)—which I define as willingness to risk relatively small expenses in
certain kinds social donations to whomever may be needy—partly because of
the prevalence of interested audiences and keenness of their observation, and
the use of beneficent acts by others to identify individuals appropriate for later
reciprocal interactions. In complex social systems with much reciprocity, being
judged as attractive for reciprocal interaction may become an essential ingredi-
ent for success. Similarly, to be judged harshly because of failure to deliver small
social benefits indiscriminately in appropriate situations may lead to formidable
disadvantage because of either direct penalties or lost opportunities in subse-
quent reciprocal interactions.
 Indirect Reciprocity } 225

I suggest that indirect reciprocity led to the evolution of ever keener abilities to
observe and interpret situations with moral overtones. In such a milieu, I would
argue, a modicum of indiscriminate beneficence would arise, as social investment,
because of benefits to individuals who are viewed as altruists. Beneficence can
approach being indiscriminate in two ways: (1) some acts can be indiscriminately
beneficent and (2) all acts, or social behavior in general, can tend in the direction
of being indiscriminately beneficent. These two different expressions of benefi-
cence will not necessarily have the same consequences for the actor.
Population-wide indiscriminate beneficence might also evolve when small
“populations” are regularly composed of relatives related to a similar degree,
and if the individuals of other populations are never contacted and therefore not
discriminated against. This may be an unlikely situation for mammals or even
vertebrates in general. This kind of indiscriminate beneficence would require no
special proximate mechanisms—no social learning; but there is yet no undisputed
evidence for unlearned recognition of relatives in any species (see reviews by
Sherman and Holmes, 1985; Alexander, 1985).
Figure 9.1 describes hypothetical social stages through which the evolving
human species might have passed (many times), and seeming to lead (but, as
argued here, probably not actually doing so) toward a utilitarian or idealized model
of morality in which all social investment becomes indiscriminate beneficence.
As already noted, complete and indiscriminate beneficence, as in the utilitarian
system of philosophers (i.e., systems promoting the greatest good to the greatest
number), would not always be a losing strategy for individuals, even in evolu-
tionary terms. Indiscriminate beneficence would not lose, for example, when the
interests of the group and the interests of the individuals comprising it are the
same. Such a confluence of interests would occur when all group members were
equally and most closely related to the individuals destined to reproduce. It could
also occur (temporarily) whenever the group was threatened externally in such
fashion that complete cooperation by its members would be necessary to dissi-
pate the threat, and when failure of the group to dissipate the threat would more
severely penalize any remaining individuals than would the group’s survival after
that individual had used all of its effort to support the group. In such cases it is not
trivial to consider the different treatments likely to be accorded those individuals
who contributed wholeheartedly and unselfishly to the well-being of the group
when it was threatened, and those who did not, or who in fact selfishly betrayed
their fellows or ignored their needs.
General encouragement of indiscriminate beneficence, and general acceptance of
its beneficial effects, results in a society with high social unity. This encouragement
and acceptance is expected to occur partly because of the likelihood, much of the
time, that nearly everyone benefits from living in a unified society (as opposed to a
socially divisive one), but also partly because individuals gain from portraying them-
selves as indiscriminate altruists, and from thereby inducing indiscriminate benefi-
cence in others (and often from inducing degrees of it that are deleterious to those
226 { Human Social Evolution

others). This means that whether or not we know it when we speak favorably to our
children about Good Samaritanism, we are telling them about a behavior that has
a strong likelihood of being reproductively profitable. In a small social group this
can be true for the Good Samaritan even if he or she is never identified, but Good
Samaritan acts seem likely to be most profitable to the actor if his responsibility for
the act is discovered accidentally, and most importantly through no effort of his own.
I would postulate that self-serving indiscriminate social investment—because
it was seen as net-cost (i.e., genetic as well as phenotypic) altruism and was inter-
preted wrongly as part of a real trend toward universal indiscriminate (net-cost)
altruism-provided the impetus for the idealized modern model of morality por-
trayed in figure 9.1. The value of self-serving beneficence, it seems to me, is what
sets the stage for the evolution of the ability and tendency to develop a conscience,
which I have interpreted (Alexander, 1979a) as the “still small voice that tells us
how far we can go in serving our own interests without incurring intolerable risks.”
The implication is that approaches to morality are expressed consistently, and
to the degree they are usually realized in society, because there is continual pres-
sure to bring about a condition of more nearly ideal morality. If so, this pressure is
likely to be applied by each individual so as to cause his neighbor, if possible, to be
a little more moral than himself. Stated differently, it would be to the advantage of
each individual in a society that other individuals, especially those not most closely
related to him, actually achieve or approach the ideal of completely moral behavior.
Ideally moral (indiscriminately beneficent) people would tend to “help” others in
the society, however slightly, to achieve the goals that evolutionists believe have
driven evolution by natural selection. They would contribute slightly to everyone
else’s interests by (1) helping their interactants directly, (2) hurting themselves in
relation to others, and (3) setting an example that others may follow, thereby con-
tributing to the interests of the group as a whole. Accordingly, one expects that
the individuals in a society would gain from exerting at least a little effort toward
encouraging other individuals to be more moral (altruistic, beneficent) than they
otherwise might have been. Among the many ways of accomplishing this is included
the setting up of an idealized morality as a model or goal, and the encouragement
of everyone (else) to become like that. One way of promoting this situation is to
designate as heroes those who approach the ideal moral condition. One expects
that sainthood may be awarded to individuals who spend their lives on explicitly
antireproductive behavior. The prevalence among saints of asceticism, self-denial,
celibacy, isolation from relatives, devotion to the welfare of strangers, and other-
wise indiscriminate tendencies to be altruistic supports this hypothesis. So does the
fact that sainthood is generally awarded (long) after the death of the awardee (thus,
the awardee cannot personally gain from this heroic designation).
The long-term existence of complex patterns of indirect reciprocity, then, seems
to favor the evolution of keen abilities to (1) make one’s self seem more beneficent
than is the case; and (2) influence others to be beneficent in such fashions as to be
deleterious to themselves and beneficial to the moralizer, e.g., to lead others to (a)
 Indirect Reciprocity } 227

100
Indiscriminate

???
INVESTMENTS IN
RECIPROCITY

Discriminate

PORTION
OF EXTENDED FAMILY
HUMAN NEPOTISM
SOCIAL
CHART

PARENTAL CARE

MATE HELP

0
Small bands in Intermediate-sized Large techno- Postualted
marginal habitats groups (tribes, etc.) logical nations changes
(Ecologically (Polygyny, cousin (Socially imposed necessary to
imposed marriages, group- monogamy, codi- an idealized
monogamy, controlled fied laws, private moral system.
little wealth, etc.) property, large property, etc.)
wealth and power
differentials, etc.)
EXAMPLES OF HUMAN SOCIAL SYSTEMS

FIGURE 9.1 A speculation about the relative importance of different kinds of social
interactions in some different kinds of societies. The principal purpose is to show
the probable origins of indiscriminate altruism, its probable significance in different
societies, and the changes from existing societies that would be necessary to realize an
idealized model of morality in which everyone was indiscriminately altruistic.

invest too much, (b) invest wrongly in the moralizer or his relatives and friends,
or (c) invest indiscriminately on a larger scale than would otherwise be the case.
According to this view, individuals are expected to parade the idea of much benefi-
cence, and even of indiscriminate altruism as beneficial, so as to encourage people
in general to engage in increasing amounts of social investment whether or not it
is beneficial to their interests. They may be expected to locate and exploit social
interactions mimicking genetic relatedness leading to nepotistic flows of benefits
(e.g., to insinuate themselves deceptively into the role of relative or reciprocator so
as to receive the benefits therefrom). They may also be expected to depress the fit-
ness of competitors by identifying them, deceptively or not, as reciprocity cheaters
(in other words, to moralize and gossip); to internalize rules or evolve the ability to
acquire a conscience, interpreted (Alexander, 1979a) as the ability to use our own
judgment to serve our own interests; and to self-deceive and display false sincerity
228 { Human Social Evolution

as defenses against detection of cheating and attributions of deliberateness in cheat-

ing (Trivers, 1971, 1985; Campbell, 1975; Alexander, 1974, 1977b, 1979a, 1982, 1985).
So we are provided with the general hypothesis that tendencies toward moral
behavior, and the establishment of moral systems, are vehicles for promoting the
goals of society as a whole: that they develop because all of the individuals of soci-
ety often share the same goals, that, ultimately, these goals involve competition
with and defense against other human groups; that, except in times of severe exter-
nal threats recognized by everyone as requiring extreme cooperativeness, the ideal
of universal indiscriminate beneficence is not met within groups; that the ideal
morality has never even been approached between societies or nations; and that,
because some degree of within-society competition probably occurs nearly all of
the time, every individual may be expected to use the impetus toward realizing
the goals of everyone to his own advantage by promoting a slightly greater degree
of “morality” in his neighbor than in himself (i.e., a net-cost or genetic altruism).
The question may be raised, however, why anyone should be vulnerable to
manipulation unduly far in the direction of beneficence, if we have been subjected
to such manipulations a very long time? Why, in other words, should moralizing
ever be effective? I think there are at least four contributing factors. First, the degrees
of beneficence that are actually reproductively appropriate will vary dramatically
as societies move between periods of extreme danger and relative security, making
it difficult to know how to behave. When will a specified degree of failure to accede
to exhortations to be beneficent cost more than it yields, because of (a) failure of
the group on which one depends for success, or (b) responses within the group to
one’s failure to be beneficent? Second, individuals may be expected to take advan-
tage of this dramatic shifting to deceive others about the degree of danger so as to
induce unduly beneficent behavior in others. Sometimes aspiring leaders may use
such deception to promote their own leadership as an antidote to the supposed
threat, and as a promoter of unity. Third, we may expect that the individuals in
a society such as we have been describing will evolve to deceive others about the
degree of beneficence they themselves are exhibiting: Everyone will wish to appear
more beneficent than he is. There are two reasons: (1) this appearance, if credible,
is more likely to lead to direct social rewards than its alternatives; (2) it is also more
likely to encourage others to be more beneficent. If one’s associates are beneficent,
then he can afford to be (or is forced to be) more beneficent than if they are not
(we may note the additional feedback from these facts that would cause everyone
to be concerned that everyone else appear beneficent so that people in general
will feel comfortable with a higher degree of beneficence than would otherwise
be the case). Fourth, if kin recognition is learned (Alexander, 1977a; 1979a; 1985a;
Greenberg, 1979; Sherman and Holmes, 1985; Mintzer, 1982), mistakes are likely,
and one may insinuate himself into the role of a relative so as to receive inappro-
priate nepotism, or even pretend to be nepotistic so as to receive the appropriate
beneficent responses. Playing upon the tendency of everyone to strive to appear
more beneficent than he is, and using the other ploys just described, may lead
 Indirect Reciprocity } 229

to much success in social manipulation. The introduction of indirect reciprocity,

whereby society as a whole or some large part of it provides the reward for benefi-
cence and the punishment for selfishness (fines for running stop signs; tax rebates
for donating to charity, etc.), simultaneously served both society and the individu-
als comprising it, and provided a vehicle for manipulating individuals socially to
levels and kinds of beneficence detrimental to them (or to their reproductive suc-
cess). It is somewhat paradoxical that the tendencies and pressures in the direction
of idealized moral systems should serve everyone in the group up to a point, but
then be transformed by the same forces that molded them, into manipulations of
the behavior of individuals that are explicitly against the interests of those being
manipulated and in the interests of those ostensibly contributing to everyone’s
interests by promoting trends toward morality in the system.
One consequence (and a saving grace) of the pressure within societies for
everyone to be a little more moral than would pay, and of keen abilities by people
in general to determine tendencies and willingness to behave beneficently or not,
is that no one can afford to lag too far behind relative to everyone else. As benefi-
cence continues to be promoted, everyone has to follow along, so that the most
selfish individuals would be forced to be less selfish, and perhaps as well variance
in readiness to be beneficent would narrow as the “front” of beneficence advances
in the direction of the ideal of indiscriminate investment and true justice in the
form of equal opportunity and equal treatment under the law. It is possible that
the societies in which moral philosophers operate have actually changed so much
in this direction during the past two or three centuries as to alter the preoccupa-
tions of moral philosophy toward a greater concern for utilitarian ideals and a less
jaundiced view of humanity. If so, there is likely no greater irony than the fact that
modern technological societies, whatever the degree of egalitarianism or approach
to the philosophical ideal of morality within some of them, are teetering us on
the brink of disaster as a result of their interactions with one another. The prob-
lem has become one of inducing between and among societies the same processes
of moralizing pressure and democratization that have developed so intricately
within them.
It is also true that, in the absence of overriding power differentials, dramatic
departures from usual levels of beneficence in the direction of serving one’s own
interests are virtually certain to result in net losses as a result of shifts of reputation
or status, or subsequently diminished beneficence from others. On the other hand,
dramatic departures from usual levels of beneficence in the direction of indiscrimi-
nateness may raise status and multiply subsequent benefits so as to produce a net
return to the actor. This asymmetry of effects would seem likely to cause acts of
cheating and selfishness to depart minimally from norms while promoting dra-
matic or extreme acts of heroism, charity, and saintliness. Perhaps, to some extent,
the asymmetry of these two effects is involved in the “creep” of certain kinds of
closely knit, stable societies toward more highly cooperative, democratic opportu-
nity-equalizing structures.
230 { Human Social Evolution

I believe that the various factors discussed here are the essential elements that
produce and maintain what we commonly call moral systems, and moral behavior
in individuals. Understanding them represents the means for resolving the exist-
ing paradoxes with respect to morality, eliminating the aura of mystery that has
surrounded the concept, and understanding not only why moral systems have
always fallen short of our ideals but why we nevertheless establish and maintain
such ideals. If accurate, these arguments may also clarify the routes by which we
can most closely approach what are seen as idealized moral systems, and perhaps
most confidently avert moral disasters.
Moral talk is often rather repugnant. Leveling moral accusations, expressing
moral indignation, passing moral judgment, allotting the blame, adminis-
tering moral reproof, justifying oneself, and above all, moralizing—who can
enjoy such talk? And who can like or trust those addicted to it? The most
outspoken critics of their neighbors’ morals are usually men (or women)
who wish to ensure that nobody should enjoy the good things in life which
they themselves have missed and men who confuse the right and the good
with their own advancement (Baier, 1965, p. 3).
Seeking to protect the autonomy that we have learned to prize, we aspire
ourselves not to be manipulated by others; seeking to incarnate our own
principles and stand-point in the world of practice, we find no way open
to us to do so except by directing towards others those very manipulative
modes of relationship which each of us aspires to resist in our own case
(MacIntyre, 1981b, p. 66).

Literature Cited

Alexander, R.D. 1974. The evolution of social behavior. Ann. Rev. Ecol. Syst. 5:352–383.
Alexander, R.D. 1977a. Evolution, human behavior, and determinism. Proc. of the Biennial
Meeting of the Philosophy of Science Association (1976), 2:3–21.
Alexander, R.D. 1977b. Natural selection and the analysis of human sociality. In Changing
scenes in the natural sciences, C. E. Goulden (ed.). 1776–1976 Bicentennial Symposium
Monograph, Philadelphia Academy of Natural Sciences, pp. 283–337.
Alexander, R.D. 1979a. Darwinism and Human Affairs, University of Washington Press,
Seattle xiv + 317 pp.
Alexander, R.D. 1982. Biology and the moral paradoxes. J. Social Biol. Struct. 5: 389–395.
Alexander, R.D. 1985a. Genes, consciousness, and behavior theory. In A Century of Psychology
as Science, S. Koch and D. E. Leary (eds.). New York: McGraw-Hill, pp. 783–802.
Alexander, R.D. 1985b. A biological interpretation of moral systems, Zygon 20: 3–20.
Alexander, R.D. 1986b. Biology and Law. In Ethology and Sociobiology 7:167–173. R. Masters
and M. Gruter (eds.).
Axelrod, R. 1984. The evolution of cooperation. New York: Basic Books.
Axelrod, R. and W.D. Hamilton. 1981. The evolution of cooperation. Science 211:1390–1396.
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Baier, K. 1965. The moral point of view: A rational basis of ethics. Abridged ed. New York:
Random House.
Brandt, R.B. 1979. A theory of the good and the right. Oxford: Clarendon Press.
Callahan, D. 1985. What do children owe elderly parents? Hastings Center Rep. 15:32–37.
Campbell, D.T. 1975. Conflicts between biological and social evolution and between psy-
chology and moral tradition. Amer. Psychol. 30:1103–1126.
Connor, R. 1986. Psuedo-reciprocity: Investing in mutualism. Animal Behaviour
34:1562–1566.
de Waal, F. 1982. Chimpanzee politics: power and sex among apes. New York: Harper and
Row.
de Waal, F. 1986. Who pays for social instability? Scapegoating in primates, and a fatal fight
in the Arnhem chimpanzee colony. Ethol. Sociobiol. 7.
Frankena, W.K. 1973. Ethics, 2nd. ed. Englewood Cliffs, NJ: Prentice Hall.
Frankena, W.K. 1980. Thinking about morality. Ann Arbor, MI: Univ. Michigan Press.
Grant, G.P. 1985. English-speaking justice. Notre Dame, IN: Univ. Notre Dame Press.
Greenberg, L. 1979. Genetic component of bee odor in kin recognition. Science
206:1095–1097.
Hamilton, W.D. 1964. The genetical evolution of social behavior, I, II. J. Theoret. Biol. 7:1–52.
Kelsen, H. 1957. What is justice? Justice, law, and politics in the mirror of science. Collected
essays. Berkeley, CA: Univ. Calif. Press.
Kohlberg, L.L. 1981. Essays on moral development. I. The Philosophy of moral development.
San Francisco, CA: Harper and Row.
MacIntyre, A. 1981b. After virtue: a study in moral theory. Notre Dame, IN: Univ. of Notre
Dame Press.
Mintzer, A. 1982. Nestmate recognition and incompatibility between colonies of the acacia
ant, Pseudomyrmex ferruginea. Behav. Ecol. Sociobiol. 10:165–168.
Perry, R.B. 1954. Realms of value: A critique of human civilization. Cambridge, MA: Harvard
Univ. Press.
Pound, R. 1959. Jurisprudence. St. Paul, MN: West Publ. Co.
Rawls, J. 1971. A theory of justice. Cambridge, MA: Harvard Univ. Press.
Richards, R. 1986b. A defense of evolutionary ethics. Biol. Phil. 1:265–293.
Sahlins, M.D. 1965. On the sociology of primitive exchange. In M. Banton (Ed.), The
relevance of models for social anthropology, pp. 139–236. London: Travistock.
Sherman, P.W. and W.G. Holmes. 1985. Kin recognition: Issues and evidence. In B.
Holldobler and S. Lindauer (Eds.), Experimental behavioral ecology, Fortschritte der
Zoologie, Vol. 31, pp. 437–460. NY and Stuttgart: G. Fischer Verlag.
Strong, C. 1984. The neonatologist’s duty to patient and parents. Hastings Center Rep.
14:10–16.
Trivers, R.L. 1971. The evolution of reciprocal altruism. Quart. Rev. Biol. 46:35–57.
Trivers, R.L. 1985. Social evolution. Menlo Park, CA: Benjamin/Cummings.
West-Eberhard, M.J. 1975. The evolution of social behavior by kin selection. Quart. Rev.
Biol. 50:1–33.
Whiteley, C.H. 1976. Morality and egoism. Mind 85:90–96.
10 }

Evolution of Human Intelligence

Reality and the Human Enterprise

Science discovers and documents reality,
at its best enthusiastically,
imaginatively, meticulously,
and necessarily dispassionately.
Music, Art, and Literature elaborate on reality,
at their best enthusiastically,
imaginatively, elegantly,
and necessarily passionately.
Politics, Law, and Morality stabilize reality,
at their best, wisely and justly.
Humor mocks reality,
at its best, constructively.
Realities can be physical,
string, particle, or wave to a universe
or biological I (animal and plant)
or biological II (human, and a special sociality).
Human social realities can be completely accurate,
because complete agreement is the only criterion.
And they can be contrary to physical realities,
deliberately, even, yet serve the believers
better than other realities, but only sometimes,
and that sometimes is when cooperation,
joining to achieve a common goal,
is required to be all that is important.
Animal and plant realities can be affected by humans,
subordinated or not to social realities.
 Evolution of Human Intelligence } 233

Human realities regarding self have so far

been subordinated to human social realities;
we have not been willing yet to know
everything about ourselves,
not the things we are evolved to suppress,
or those that seem to make us unhappy;
not the self-deception we use to further our own
desires and goals, and that generates social reputations
but only temporarily and shakily accurate versions.
Art, Music, Literature,
Politics, Law, Morality,
and Humor, too, are restricted
to the human social kind of reality.
Mocking individual realities can
save the humorist too,
but only when it works
for him in the eyes of others.
Failing that,
the effort buries him.
But a humor that mocks
social and political realities
may also save the world.
Alexander, 2011, p. 260
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 INTRODUCTION

Reflections on the Evolution of the Human Psyche

R.I.M. Dunbar

Commentary on: R. D. Alexander (1989). Evolution of the human psyche.

In: P. Mellars & C. Stringer (eds.) The Human Revolution, pp. 455–513.
Edinburgh University Press.

The edited volume The Human Revolution was published in 1989 with the aim of
summarizing the background to the appearance of modern humans. Dick Alexander
contributed a lengthy piece to this volume on the evolution of the modern human
mind—in effect, what it is to be human and how we came to be that way. His article
(it is 60 pages long) divides naturally into three basic components. The first part sets
out the background and agenda, and argues a trenchant case for the claim that the
origins of the human mind lie in the social domain. The second part is as an interlude
and revisits the thorny old debate surrounding the application of evolutionary theory
to human behavior and psychology—a reflection, perhaps, of the fact that, barely a
decade after the “Sociobiological Revolution,” the vitriolic debate that had followed
the publication of Ed Wilson’s Sociobiology and Dawkins’s Selfish Gene was still alive
and kicking. (Sadly, although things are much improved in this respect three decades
on, a deep-rooted antipathy to Darwinian ideas still colors attitudes in some parts
of the humanities and social sciences.) The third part is the heart of the paper and
addresses the question of how and why the human mind came to be so different. Dick
placed a strong emphasis on this in the paper: The “cultural” activities of animals not-
withstanding, humans are in a different league to everyone else in that they do things
(like building cathedrals and writing plays) that no other species does.
The essence of his argument is summed up in a three remarkably prescient
sentences at the outset of this third section:

I think the key argument . . . . is that consciousness represents a system of

(1) building scenarios or constructing possible (imagined) alternatives; (2)
testing and adjusting them according to different projected circumstances;
and (3) eventually using them according to whatever circumstances actually
arise. [In a previous paper] I referred to such abilities as the capacity to over-
ride immediate rewards and punishments in the interests of securing greater
rewards visualized in the future. . . . In this view, consciousness, cognition,
and related attributes—which probably represent the core of the problem in
236 { Human Social Evolution

understanding the human psyche—have their value in social matters, and

the operation of consciousness can be compared to the planning that takes
place in a game in which the moves of the other players cannot be known
with certainty ahead of time. (p. 477)

Play loomed large in this argument, but for Dick it had a special meaning over
and above the more conventional interpretation of play as physical practice: cen-
tral to his argument was what he termed “social/intellectual play,” the capacity to
ruminate on and mull over alternative scenarios in the light of others’ possible
responses to one’s actions. Play, in his view, allowed individuals to learn how to
predict others’ strategic responses as adults, and so gave rise to the human capacity
to evaluate the outcomes of alternative courses of action and thus choose between
them more effectively—a capacity sometimes subsequently referred to as “mental
time travel” (Barrett et al., 2003; Suddendorf et al., 2009).
In a singularly influential paper published a decade earlier (Alexander, 1974),
Dick had argued that the evolution of group-living in primates (and other species)
arose in response to one of two core problems: defence against predators or the
opportunity to monopolise resources. Both these suggestions were taken up by
others in later decades (e.g., van Schaik, 1983, Wrangham, 1980) and they continue
to exercise debate even today. However, in his Human Revolution contribution,
Dick eschews resource defence as a likely selection factor for group living and
comes down hard in favour of predation risk. Resource defence, he argues, could
only have arisen after group living had come about, and so must be a consequence,
not a cause, of group living. In this respect, his arguments have largely been borne
out, at least in the case of primates and ungulates (see, e.g., Shultz and Dunbar,
2006; Adamczak & Dunbar, 2008).
Predation as the driver for group living is the bedrock on which Dick built
his argument. The key steps can be summarized as: predation selects for living
in groups; living in groups inexorably gives rise to competition between groups
(thus, opening up the opportunity for resource defence); such competition selects
for the capacity to cooperate in mounting a defence (or attack) against rivals over
resources; cooperation selects for consciousness (i.e., the cognitive abilities needed
to manage effective group-level cooperation), which in turn selects for increased
brain size etc. The problem to be solved was, as he put it:

[W]hat kinds of mechanisms enabled group-cooperative humans to conduct

intergroup aggression cooperatively. How did humans manage the coordi-
nation necessary to carry out raids efficiently, especially against enemies
belonging to their own species and possessing the same general abilities and
tendencies? (p. 498)

In the article, Dick makes a great deal of kin selection and tactical deception
in this respect—something that was perhaps inevitable given that it was writ-
ten in the immediate aftermath of the launch of the Machiavellian Intelligence
 Evolution of Human Intelligence } 237

Theory of primate brain evolution (Byrne & Whiten, 1988) and an increasing
interest in the evolution of deception (e.g., Krebs & Dawkins, 1984). Kin selec-
tion, of course, remains a central plank in all evolutionary analyses, but the
Machiavellian Intelligence Hypothesis has mutated into the softer form of the
Social Brain Hypothesis (Dunbar, 1992a, 1998; Barton & Dunbar, 1997) in which
affiliative bonding (and/or social learning) is emphasized at the expense of the
deviousness implied by the term “Machiavellian” (Dunbar, 2011). Nonetheless,
deception remains, of course, an important issue in evolution, as evidenced by
the fact that it has spawned a number of important counter-strategies in terms of
human cognitive evolution (notably the cheat detection mechanisms of Cosmides
[1989; Cosmides & Tooby, 1992]). Re-reading the original text, however, reminds
me how much it anticipates the emergence of theory of mind (or mentalising) as a
central theme both in child development and in primate comparative psychology:
[One of] the most effective ways to deal with human competitors [is] . . . . the
ability to see ourselves as others see us, so as to cause them to see us as we
would like them to rather than as they would like to. The human psyche is
evidently evolved to excel at such practices” [i.e., “the ability to see ourselves
as others see us”]. (p. 491)
If this isn’t an explicit reference to theory of mind, it’s hard to see what else it
could be.
This emphasis on the importance of cooperation in animal and human social
evolution has, over the past decade or so, given rise to a minor industry in both
experimental and modelling studies of the conditions under which coopera-
tion can arise, with the numbers of papers generated by this theme running into
many hundreds. For myself, however, I found his appreciation of the fundamental
importance of the need for community cohesion in human evolution particularly
prescient. Contemporary versions of the Social Brain Hypothesis place a singular
premium on the problem of freeriders, the effect these have on destabilizing the
kinds of implicit social contracts on which cooperation necessarily depends and
the mechanisms needed to prevent freeriders from overwhelming cooperators
(Enquist & Leimar, 1993; Nettle & Dunbar, 1977; Dunbar, 1999, 2009a). Prominent
among the mechanisms being discussed in the contemporary literature are ethnic
markers and the role of religion, both of which are explicitly mentioned by Dick:
Acceptance of unifying myths or information or goals depends on the indi-
vidual’s acceptance of the value of group unity, including the position or
status of himself that will result, or other effects on himself and his intimates
(children, spouse, relatives, reciprocants). Even myths widely regarded as
counterfactual may be accepted, repeated, and elaborated if their effect is
seen as [socially] unifying. (p. 493)
My own view has come to be that the central problem we have faced through-
out our evolutionary history has been how to neutralise the destructive effects
238 { Human Social Evolution

of freeriders as we have sought to push social community size above the limits
set by social grooming (the standard mechanism that primates use to bond their
social groups) (Dunbar, 1992b, 2008). There are two related issues here. One is
the fact that time constraints impose what amounts to a glass ceiling at around 50
(the mean group size typical of the most social of the monkeys and apes, includ-
ing baboons and chimpanzees) on the number of individuals with whom one can
form coherent relationships. The second is that as community size increases, so the
pressure to defect on the social contract that underpins primate sociality increases
proportionately. If some mechanism is not found to counteract this effect, the
community will collapse back to the minimum size that primates can maintain by
grooming. A solution to the first problem has to be able to solve the second.
What is needed is some process that effectively bridges across that barrier to
reach more individuals, and laughter, music and religion (or at least the ritu-
als of religion) appear to have been the mechanisms of choice—mainly because
all three are extremely good at triggering the release of endorphins (the same
mechanism that allows grooming to be an effective mechanism for social bond-
ing: Dunbar, 2009a, 2010). This almost certainly has a long history, building suc-
cessively through these three processes from around two million years ago (the
first appearance of the genus Homo and the point at which the grooming time
constraint first kicks in) until the appearance of fully fledged religion and lan-
guage with the advent of anatomically modern humans around 250,000 years ago
(Dunbar, 2003, 2009b). With the advent of language, shared myths (or world-
views) come to play a central role during the course of later human evolution
because language allows us to coordinate religious rituals and provide them with
a meaningful raison d’être.
Central to this process is emotion, not least because endorphins have a positive
effect on affect and are responsible for creating that sense of wellbeing and warmth
that goes with successful social interactions (Zubieta et al., 2003). Dick makes a
great deal of emotion and, unusually perhaps for an evolutionary biologist, of the
physiological processes that underpin emotions. However, his discussion is largely
couched in terms of the manipulation of others’ emotions in order to deceive
them—or avoid being deceived by them. As he saw it:

Once individuals became capable of recognizing emotional states in other

individuals, then it seems virtually certain that selection would alter both
this ability and the emotional states themselves, or the external evidence
of them, in ways that would be called communicative. . . . This is the point
(in evolution) at which it would become important for us to know about
our own “feelings” or emotions—because we could then manipulate them to
affect use by others of evidence about them.

It has taken a long time, but emotions have finally begun to loom large in
discussions of human cognitive evolution (see, for example, Gamble et al., 2011;
Gowlett et al., in press).
 Evolution of Human Intelligence } 239

The key to all this lies in a growing intensity of inter-group conflict, giving
rise, in effect, to a perpetual state of war between neighboring groups. War was
undoubtedly out of fashion in the 1980s, notably among archaeologists and paleo-
anthropologists who tended to take a rather benign view of human psychology
and behavior (Keeley, 1996; Wrangham & Peterson, 1997). However, war has
begun to surface as a likely driver of human demographic and psychological evo-
lution and is currently undergoing a major resurgence of interest among evolu-
tionary biologists and psychologists (Bowles, 2009; Mathew & Boyd, 2011; Gneezy
& Fessler, 2012).
Persistent states of conflict of this kind imply competition for resources, and
that in turn implies high population densities. Indeed, it is difficult to imagine why
neighboring communities should behave aggressively toward each other in the
absence of competition for resources, since the costs of war are inevitably rather
high. One question that troubled Dick was whether human paleo-populations had
ever been dense enough to instigate significant competition between groups. The
word on the street among paleoanthropologists tended to be “No”. Resources were
in plentiful supply, population densities low and many (if not most) populations
were continually expanding into new territories. Dick felt obliged to conclude that:

densities per se [are] not critical [to my argument], or else that estimates of
densities [are] wrong. It is probably more important to know what kinds of
social groups people lived in, and why, than to know densities per se.

However, maybe there was an alternative explanation. For ecologists, the term
resources inevitably means ecological resources. This need not always be so, of
course, since women remain a potentially limiting resource for men. Males might,
therefore, compete to defend land in order to monopolize access to women, or
compete to defend groups of females, rather than defend land for the sake of the
food resources it contains. If competition was for women rather than ecological
resources, this might have solved the problem that troubled Dick. Competition
for women could in principle generate just the kind of arms’ race that his hypoth-
esis requires. Although it is not always clear what motivates warfare in small scale
societies, women are often a trophy of such activity (see, for example, Chagnon
1968) and might be seen as the ultimate objective even where the causus belli is
something more mundane. However, this is, I think a minor issue. The fact, as
Dick himself was at pains to point out, is that traditional societies revolve around
an in-group/out-group effect in which those from other communities are invari-
ably viewed with suspicion and as game for exploitation.
Interestingly, in an aside, he was “led to wonder—entirely without empirical
evidence—whether or not orangutans and gorillas once lived in social groups
more like those of chimpanzees and humans than is presently the case—in other
words, in larger multimale groups, “perhaps multi-male groups in which the males
were cooperative in hunting, or even in intergroup aggression” (p. 502). The specu-
lation turns out to have some validity. In the models that we have developed of
240 { Human Social Evolution

great ape socioecology—models that use the time costs of foraging to model the
constraints on social group size—it has become clear that gorillas and orangutans
represent alternative solutions to the chimpanzees’ problem of coping with the
ecological costs of sociality (Lehmann et al., 2008; in press). The orangutan’s soli-
tariness is simply the limiting condition in the chimpanzee’s attempt to dissipate
the costs of large social communities through a fission-fusion form of social orga-
nization, while the gorilla seems to represent an attempt to solve the same problem
by increasing body size and shifting to a more folivorous diet. Once, both almost
certainly had the same social system as the chimpanzee.
One central question remains outstanding: why have only humans, of all the
many species of primates and other mammals, needed to go so far in evolving
their unique psyche? Associated with this are the subsidiary evolutionary ques-
tions as to what was the trigger for all this and when exactly did these traits first
appear? These tantalizing questions remain as opaque now as they were in 1989.
Whatever happened on the long road from our common ancestor with the great
apes some eight million years ago to the final appearance of modern humans
around a quarter of a million years ago, the history of brain evolution in our lin-
eage suggests that it probably happened quite late—during the last 800,000 years
marked by the appearance of archaic humans. In looking for potential drivers of
evolutionary change around this time, the most obvious feature of this period is
the onset of climatic instability with rapid fluctuations between cold and warm
periods that eventually give rise to increasingly deep ice ages. The cool, dry condi-
tions that prevailed even in the tropics must have been very challenging for these
early humans, requiring novel strategies to cope with them.
Like all ecologists, paleoanthropologists tend to reach instinctively for the for-
aging innovations solution. After all, the Paleolithic record provides us with more
handmade stone tools than anything else, and, at the very least, tools imply the
dismembering of carcasses. So conventional wisdom assumes that early humans
survived because they evolved the intellectual skills to respond with novel ways of
extracting nutrients from an increasingly challenging environment. But the ques-
tion is whether these solutions to the challenges of survival related solely to forag-
ing strategies (and, hence, essentially involved individual trial-and-error learning)
or to something more social as implied by the Social Brain Hypothesis (such as
mutual exchange networks that allowed communities to gain access to others’ for-
aging territories as a buffer against local environmental catastrophes). It is difficult
to see anything in the first option that would demand the doubling of brain size that
occurred during the last half-million years of human evolution. Certainly, as Wynn
(1988) pointed out at around the time Dick was writing his article, the toolkits man-
ufactured by successive populations fail to suggest that the answer lies in techno-
logical inventiveness (see also Gowlett et al., 2012). While brain volume increased
exponentially through time, tool quality improved on something closer to a power
curve: tools hardly changed in appearance or quality for the first nine-tenths of the
period, and then underwent a dramatic development from about 50,000 years ago
 Evolution of Human Intelligence } 241

in a dazzling display of technical expertise—the very phenomenon that attracted

attention as the “Human Revolution” of the title of the volume in which Dick’s
paper was published. Meanwhile, if we are to believe the quantitative implications
of the Social Brain Hypothesis, community sizes would have been increasing in the
same exponential fashion as brain volume. Bigger groups mean more stress, both
in ecological terms and, more importantly perhaps, in social, reproductive, and
demographic terms.
Why would one need such large social groups if it was not to provide social
solutions to the ecological problems that these early humans faced? The answer
must surely have been a form of ecological buffering that exploited extended social
networks whose geographical extension was sufficient to provide access to areas
that still had resources even in the worst of times. Extended networks of this kind
would surely have provided exactly the kinds of competitive regimes that Dick
envisaged in his model, especially under environmental conditions in which pop-
ulations frequently faced resourcing challenges. If so, then it implies that Dick’s
warfare hypothesis is of relatively recent origin.
In sum, then, the 1989 article has stood up remarkably well to the passage of
time. One can always criticize the details, but these are issues that Dick had to
make the best of with the rather more limited knowledge available to us 20 years
ago. Hindsight is always a wonderful thing. The main theme of his argument,
in contrast, appears to be in good shape and as robust as it was when it was
fresh ink on the page. Yet, despite this and all the research that has been done
since 1989, one question remains obdurately unanswered: Just why are humans
so different from other species of animals? While we are beginning to unpack
the mechanistic explanations that provide an answer to how we are different
(the neuropsychology of mentalising competences, for example), there is still
no obvious answer to why we needed these competences, what environmental
conditions selected for them, and when exactly these evolutionary events were
set in train. These tantalizing questions remain to be solved by those who follow
in Dick’s footsteps.

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 EVOLUTION OF THE HUMAN PSYCHE
Richard D. Alexander

Alexander, R.D. Evolution of the Human Psyche 1989. In P. Mellars and C. Stringer
(eds). The Human Revolution. Behavioral and Biological Perspectives on the Origins
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The gap (between us and our nearest living relatives, the apes . . . ) is largest,
and most difficult to comprehend, in terms of mind . . . As human beings are
distinguished so much by their minds, . . . those minds must be a legitimate
object of evolutionary studies (Gowlett 1984: 167 and 188).

Introduction

The purpose of this essay is to develop and test hypotheses about the process
and pattern by which the human psyche evolved, and to seek to understand why
humans, and humans alone, differ strikingly in mentality from their closest rela-
tives—and evidently from all other organisms. Understanding the human psyche
is a key to understanding human sociality (1) as it relates to the behaviour of indi-
viduals in different circumstances and after different kinds of learning experiences
or developmental events and (2) as it yields variations in cultural patterns in differ-
ent environments, and following different histories, including extreme and com-
plex phenomena such as the rise of nations.
By the human ‘psyche’ I mean the entire collection of activities and tendencies
that make up human mentality. I include concepts such as (1) consciousness and
all of its correlatives or components, such as subconsciousness, self-awareness,
conscience, foresight, intent, will, planning, purpose, scenario-building, memory,
thought, reflection, imagination, ability to deceive and self-deceive, and represen-
tational ability; (2) cognition (i.e. learning, logic, reasoning, intelligence, problem-
solving ability); (3) linguistic ability; (4) the emotions (grief, depression, elation,
excitement, enthusiasm, anger, fear, indignation, embarrassment, despair, guilt,
uncertainty, etc.); and (5) personality traits (stubbornness, pliancy, subservience,
timidity, persistence, arrogance, audacity, etc.).
One can analyse human mentality by (a) morphological and physiological stud-
ies of the brain and its functions; (b) psychological and psychoanalytical investiga-
tion of behaviour and its underlying motivations and other correlates; (c) inquiries
into artificial intelligence, including modelling with machines or mathematics;
(d) archaeological and anthropological analysis of fossils and artifacts (focusing
 Evolution of Human Intelligence } 245

primarily on the most direct possible evidence and the pattern of evolutionary
change); or (e) comparative study of humans and other animals, especially close
relatives, combined with adaptive modelling (utilizing primarily predictiveness
from knowledge of the process of evolutionary change). The last method is the one
principally employed here.
First, a unique selective situation is postulated to account for humans depart-
ing as far as they have, psychically and in other regards, from their closest living
relatives, and it is compared to alternative hypotheses. The human psyche is then
characterized in terms of the probable reproductive significance of its different
aspects, thereby generating additional hypotheses about its selective background.
Finally, an effort is made to test the hypotheses generated by the first and second
parts of the discussion.

The Postulated Selective Situation

BACKGROUND OF THE HYPOTHESIS

There is probably general agreement that explaining human evolution is to a

large extent a question of understanding how human mental attributes evolved.
The problem is not only why brains evolved to be bigger and intellects to be more
complicated, but also why they became so dramatically different from those of our
closest living relatives. Humphrey (1976) suggested that the selective situation was
primarily a social one, with evolving humans providing their own selective chal-
lenge; as with others who have made suggestions in this direction, however (see
references below), he did not explain what forces caused humans to continue to live
under the social conditions responsible for the expenses of intense competition and
the resultant manipulations, deception, and favouring of social cleverness that he
and others postulate. Thus, he did not account for the fact that humans alone have
followed an evolutionary pathway leading to what he called a ‘runaway intellect’.
Humans are not just another unique species, rather they are unique in many
and profound ways—that is, in many attributes, and also in ways that unexpect-
edly set them apart from all primates, all mammals, or even all life (e.g. Alexander
and Noonan 1979; Tooby and DeVore 1987; Wilson 1975; Wrangham 1987). For
example, rapid evolution usually means more speciation, but humans, whose
brains are regarded as having evolved according to an ‘autocatalytic’ model—
increasingly rapidly—during at least the past two million years (Godfrey and
Jacobs 1981; Stringer 1984), have no living close relatives. By this I mean that there
are no closely similar or sister species, no congeneric species, no interfertile spe-
cies, no species, even, with the same number of chromosomes. Why? Why do we
have to go back two, five (or more) million years to find the most recent phyloge-
netic juncture with our nearest living relatives (Ciochon 1987)?
Human social groups are also unique (currently) in being huge and socially
complex, while also having all individuals both genetically unique (excepting
246 { Human Social Evolution

monozygotic twins) and expecting to reproduce; and only humans (apparently)

play competitively, group-against-group (currently on a large scale). Although we
became a virtually world-wide, highly polytypic species with numerous geographic
variants, until recently those different variants have not easily mixed or lived in
sympatry; and there seems to be no universally accepted evidence that multiple
species of hominids ever lived together. With increases in the world population of
humans, moreover, we did not come to live in a single, huge, dense, amorphous,
universally beneficent population; rather, we have always lived with tense national
boundaries, patriotism, xenophobia, and almost continual and destructive inter-
group competition and conflict. Today we have a terrible international arms race
as a central horror in our lives. We have at least been primed by evolution so as to
allow these things to happen. How were we so primed?

COMPONENTS OF THE HYPOTHESIS

A. The most unpredictable and demanding aspects of the environment of

evolving humans have always been its social aspects, not the physical cli-
mate or food shortages, as is often implied. The human psyche was designed
primarily to solve social problems within its own species, not physical and
mathematical puzzles, as educational tests and some concerns of philoso-
phers might cause us to believe. Darwin (1859, 1871), Keith (1949), Bigelow
(1969), Wilson (1973), Hamilton (1975), Alexander and Noonan (1979),
and Alexander (1967–1988) have all suggested some parts or versions of
this model, but Humphrey (1976) probably described it most clearly (inde-
pendent hints toward it are also numerous—e.g. Trivers 1971; Fox 1980;
Kurland and Becker 1985; Box and Fragaszy 1986; Burling 1986). This
hypothesis implies that even the solving of mathematical, physical, and non-
human biotic problems had its central significance (in the broadest sense, its
reproductive rewards) in social contexts. (For example, Lenneberg (1971)
argues that ‘mathematical ability may . . . be regarded as a special case of
the more general ability that also generates language . . .’ and Burling (1986)
that ‘the . . . evolution of the . . . capacity to learn and use highly complex lan-
guage is unlikely to be explained primarily by any subsistence or techno-
logical advantages that language offers. Rather, language probably served
social purposes’.) In other words, this hypothesis rejects the notion that
complex intellects evolved because they saved early humans from starva-
tion, predation, climate, weather, or some combination of such challenges.
All other organisms have solved these kinds of problems, in a variety of
ways, without complex human-like intellects. If humans solve such ordi-
nary problems in extraordinary ways, I am suggesting, it is because they
are using an intellect evolved in a different context (For comparative pur-
poses, Isaac (1979) lists six hypotheses bearing on human evolution: Dart’s
 Evolution of Human Intelligence } 247

(1949, 1954) ‘hunting’ hypothesis; Jolly’s (1970) ‘seed-eating’ hypothesis;

Tanner and Zilman’s (1976) ‘gathering’ hypothesis; Isaac’s (1978) ‘food-
sharing’ hypothesis; Parker and Gibson’s (1979) ‘developmental’ hypothesis,
based primarily on food skills; and Lovejoy’s (1981) ‘shortened birth inter-
val’ hypothesis). Dart’s is the closest to that espoused here; the others all
depend on non-human biotic or physical threats as primary forces. As I am
restricting it, my hypothesis also requires that human proficiency in tool
construction and use is also a secondary or incidental effect of the evolution
of an intellect designed to be effective in social contexts. Wynn (1979) and
Gowlett (1984) discuss the relationship between the manufacture of tools,
and especially the transport of materials involved in their construction, to
the evolution of planning and foresight. In this connection it is relevant that
chimpanzees show evidence of planning, and perhaps scenario-building, in
such tool-using behaviour as the selection, preparation and carrying of ter-
miting sticks (Goodall 1986; Ghiglieri 1988). It is obviously important to
my hypothesis that they also seem to show considerable foresight in social
activities (Goodall 1986; Ghiglieri 1988).
B. Human mental abilities evolved as a result of runaway social compe-
tition, an unending within-species process dependent upon interminable
(and intense) conflicts of interest, compared (below) to Fisher’s (1958) con-
cept of runaway sexual selection (see Alexander 1987).
C. Balance (or imbalance of power races) between social groups, either
within or between (very similar) species, facilitated runaway social com-
petition by favouring complex social living, and abilities to behave coop-
eratively and competitively within (and between) social groups. Such races
‘trapped’ humans into social interdependence, led to within-group amity
and between-group enmities, and in part created the selective situation that
gave rise to our creative intellects. Humans may not be the only species to
engage in social reciprocity and cooperation-to-compete (with conspecif-
ics), but they are probably the only one in which this combination of activi-
ties is a central aspect of social life.
D. These processes became paramount partly because the ecological
dominance of evolving humans diminished the effects of ‘extrinsic’ forces of
natural selection such that within-species competition became the princi-
pal ‘hostile force of nature’ guiding the long-term evolution of behavioural
capacities, traits, and tendencies, perhaps more than in any other species.
The evidence for this having happened is the current ecological dominance
of humans; the only problem is when and how it came about. One might ask
if (1) the ecological dominance of humans allowed the evolution of complex
intelligence or (2) complex intelligence enabled humans to become ecologi-
cally dominant. I would argue, rather, that the two went hand in hand, rein-
forcing one another at every stage, and I suggest (below) that, aside from
the human presence, chimpanzees may already have attained the required
248 { Human Social Evolution

dominance.
The reference to ‘extrinsic forces’ above is to Darwin’s Hostile Forces of Nature –
parasites, predators, diseases, food shortages, climate, and weather—as an exhaus-
tive list of the features of natural selection that determine the reproductive success
and failure of different genotypes. Darwin (1859, 1871) distinguished between nat-
ural selection and sexual selection, so he did not include in the list, as I do, mate
‘shortages’ (meaning, ultimately, variations in mating success, including quality as
well as quantity of mates). Darwin’s emphasis on sexual selection to account for
the evolution of many human traits is in accord with the idea presented here, if the
context is expanded to include other kinds of social competition, and I believe that
the current idea supports his general suggestion.
E. The combination of (1) balance-of-power races between human social
groups, (2) runaway social competition and the emphasis on creative and
manipulative intellects, allowed or facilitated by (3) human ecological domi-
nance, can also be used to help explain the changes in social structure that
occurred as human social groups expanded toward their present sizes and
took the forms (bands, tribes, and nation-states –‘egalitarian’, despotic, total-
itarian, or democratic societies) represented across human history.
F. The central evolved function of the human psyche, then, is to yield an
ability to anticipate or predict the future—explicitly the social future—and
to manipulate it in the (evolutionary, reproductive) interests of self ’s genetic
success. In the hypothesis developed here, all other effects or properties of
the psyche are secondary to this strategic function. This general situation
came about because evolving humans (a) came to live in highly cooperative
social groups and (b) became ecologically dominant, these two conditions
together (i) reducing the significance of hostile forces of nature other than
conspecifics and (ii) leading to cooperation to compete against conspecifics
who were doing precisely the same thing. In this fashion the combination
of an unending runaway social competition and an unending balance-of-
power race was set in motion, which continues within and among human
populations today. This general situation allowed and caused the radical
departure of humans from their closest relatives, in psychical and other
attributes.
A central feature of the human psyche is the construction of alternative scenar-
ios as plans, proposals, or contingencies in a manner or form perhaps appropriately
termed social-intellectual practice for social interactions and competitions (prac-
tice which lacks a prominent physical component). This hypothesis of scenario-
building sheds light simultaneously on a collection of human enterprises that have
seemed virtually impossible to connect to evolution—such as humour, art, music,
myth, religion, drama, literature, and theatre—because they are involved in sur-
rogate scenario-building, a form of division of labour (or specialization of occu-
pation) that may be unique to humans (partly because language is required for
 Evolution of Human Intelligence } 249

communication of mental scenarios between individuals). The centrality of sce-

nario-building in human sociality (which will be related to the concept of play) is
connected with the appearance of rules (hence, moral and legal systems) through
(in part) the value of limiting the extent to which the elaborate and expensive
scenarios (plans) of others can be thwarted by selfish acts (Alexander 1987, see also
below). Finally, part of the game of human social competition involves conceal-
ing how it is played, and some of such concealment involves concealing it from
one’s self (self-deception). This in turn compounds the problem of understanding
ourselves because of the difficulty of bringing into the conscious items that have
been kept out of it by natural selection, most particularly items involving social
motivations.
The hypothesis assumes that some version of these social functions initially
drove the evolution of consciousness and other aspects of the human psyche,
and that other uses of the psyche, such as in predicting or dealing with aspects
of the physical universe, are (or were initially) incidental effects (in the evolu-
tionary sense). This scenario does not preclude adaptive functions of the psyche
in dealing with nonsocial phenomena throughout human evolution, only that
such functions could not have caused the evolution of consciousness, cogni-
tion, linguistic traits, and the emotions as a set of human attributes. The empha-
sis on manipulation and deception is because the hypothesis holds that the
human psyche would not have evolved in a world dominated by truth-telling,
so that its complexity is tied to its use in deception. Once efforts at deception
are widespread, successful, and complicated, truth-telling also becomes difficult
to identify or prove. The argument is that truth is approached only when neces-
sary—that is, cost-effective.

GENERAL COMMENTS ON NATURAL SELECTION

Ultimately, there must be compatibility between our view of the functions of the
human psyche and our understanding of the selective background that gave rise to
it. I am going to develop the argument from the beginning, because there can be
no agreement, or adequate evaluation of arguments, unless common ground has
been established from the outset.
If we accept the view of modern biology that natural selection is the principal
guiding force of evolution, this means, first, that to understand traits we must con-
centrate on their reproductive significance and discard most of the old notions
about adaptive function, such as survival of the individual (at all cost—i.e. even
when survival is opposed to reproductive success), benefit to the population or
species (again, when there is conflict with benefit to the individual’s reproduc-
tion), progress, or any kind of goal-oriented or orthogenetic trend. We are not
free to assume that genetic drift or other random events can account for elaborate
attributes, just because they seem to give an unprejudiced, amoral, or value-free
250 { Human Social Evolution

aspect to evolution or because they can account for minor differences between
populations (Alexander 1979, 1987).

RULES FOR APPLYING SELECTIVE THINKING

Continuing from this initial assumption, I assume five general rules in applying
natural selection to the attributes of organisms (for the first two, see Williams 1985):
First, we must consider the question of adaptation, not according to some
notion of optimality or ends to be achieved, but rather according to the now
widely accepted usage, from Williams (1966), of simply better versus worse
in the immediate situation. This view implies that long-term trends occur
because particular selective forces remain in place for long times, so that
step-by-step small changes sometimes give a false retrospective appearance
of goal-oriented or orthogenetic trends. As Williams (1966) emphasized, we
must also distinguish between incidental effects of traits and their evolved
functions or evolutionary ‘design’.
Second, natural selection must always work from ‘last year’s model’—a
fact often referred to by modern biologists under concepts like phyloge-
netic and ontogenetic inertia, or structural laws of development and evolu-
tion. This particular rule implies that phenomena like allometry or neoteny
are in general maintained as a result of selection and not in spite of it; that
when such phenomena cause some kinds and degrees of evolutionary ‘iner-
tia’, they must be presumed to have developed the potential for such effects
as a result of past selection. To invoke physiological, developmental, or
phylogenetic constraints to explain evolved phenomena is thus an argu-
ment of last resort.
Third, random events such as mutations and drift introduce noise into
the adaptive process but do not guide long-term directional change.
Fourth, selection is more potent at lower levels in the hierarchy of
organization of life (Williams 1966, 1985; Hamilton 1964, 1975; Lewontin
1970; Dawkins 1976–1986; Alexander and Borgia 1978; Alexander 1979,
1987), so that, as Williams (1966) first argued convincingly, ‘most of the
characteristics of organisms, including social behaviour, must be the
result of differential fitness at the level of individual genotypes’ (Lewontin
1966).
Fifth, to understand traits, it is effective, and parsimonious, to seek or
hypothesize singular selective causes (or contexts or changes) in evolu-
tion, as opposed to accepting multiple ones too readily. This is so because
(1) it is difficult to falsify individual causes when multiple contributing
factors are accepted uncritically; (2) single causes can be sufficient, even
when multiple contributory factors are known; and (3) once a particu-
lar event, such as group-living, has occurred, then secondary effects will
 Evolution of Human Intelligence } 251

appear that (especially without attention to the possibility of single suf-

ficient causes) can be confused with the primary cause (in other words,
single different causes may occur in sequence without violating these
arguments).
Hypothesizing singular causes, I believe, is a way of making one’s ideas maxi-
mally subject to falsification, if they are incorrect, and therefore of advancing
knowledge most effectively. It is a way of going most forcefully after the actual
driving forces in evolutionary change, and of unravelling most quickly and com-
pletely the actual patterns of change. This ‘rule’ for applying selection is the most
controversial one, and the controversy arises primarily because some see it as a
way of over-simplifying causation in human social affairs. This criticism, in turn,
is prevalent among those who believe that knowledge (or supposed knowledge) of
history yields ideology for the future. This problem arises in large part out of igno-
rance about the relationship between genes and phenotype, heredity and devel-
opment, rigidity and plasticity in expression of behaviour. It cannot be erased,
however, by emasculating the procedures of science. Rather, it must be removed
from importance by explaining why the argument that history justifies ideology
cannot be sustained.
I have given no rules regarding the mechanisms by which the phenotype is
acquired, such as learning or maturation. There are two reasons: First, the opera-
tion of natural selection can be understood without knowing about, implying, or
eliminating any particular ontogenetic or physiological mechanisms. Second, pre-
dictions about expected proximate mechanisms in particular evolutionary situa-
tions are extremely difficult and complicated. Although ignorance about design
mechanisms makes it more difficult to be Confident about interpreting function,
so long as no particular restrictions are assumed (e.g., that a behaviour is ‘innate’,
learned in some particular fashion, etc.), analysis of such mechanisms can usually
be postponed without necessarily causing error.

GROUP SELECTION
Group selection (versus selection at lower levels in the hierarchy of organization
of life: Alexander and Borgia 1978) is an issue that is central, yet seems to remain
complex and confusing. Two different situations may be implied by the term
‘group selection’. The first appears to be relatively unimportant, for the reasons
given. The second is the one to which I referred (Alexander 1974) when I suggested
that humans are an excellent model for group selection (see also Alexander and
Borgia 1978).

1. Group Selection when there are Conflicts of Interest between Individual

and Group Levels. In this kind of selection, the spread or maintenance of
alleles is determined at group levels, regardless of conflicts of interest within
groups, because selection at the group level is simply more powerful than
252 { Human Social Evolution

that at lower levels. In other words, the maintenance and spread of alleles
is determined primarily by the differential extinction or reproduction of
groups, regardless of what is happening at individual or other levels. This is
the kind of selection that Wade (1976, 1978), D. S. Wilson (1975, 1980), and
others seek to validate theoretically (as feasible or likely in natural popu-
lations) and demonstrate in laboratory experiments. Their work, however,
actually indicates that group effects are weak in the face of the strength of
selection at lower levels (Williams 1985; Dawkins 1986; Alexander 1987).
Thus, to create potent group selection they have been forced to postulate
populations with attributes much like those of individuals. They invoke
groups that are founded by one or a few individuals (thus as near as possible
to being single broods of offspring), and last about one generation (thus
have the same generation time as individuals). In the laboratory they create
populations (sometimes highly artificial) with minimal within-population
genetic variance and maximal between-population genetic variance. The
effort is to maximize genetic variance and minimize generation time at pop-
ulation levels, because the intensity of selection depends on these attributes
(Fisher 1930; Lewontin 1970), which are virtually always more favourable to
selection at lower levels. There are multiple indications, in the behaviour and
life histories of organisms, that this kind of group selection does not often
prevail (Williams 1966; Alexander 1979, 1987).
Group selection that is weaker than individual selection may often affect the
rate of selective change as a result of the differential reproduction of individuals,
but group selection probably is only rarely potent enough to affect the direction
of selection within species in natural situations when it runs counter to selection
at lower levels. Selection that results in one of two competing species becoming
extinct is this kind of group selection, but such interspecies selection occurs under
conditions when the differences between groups cannot be compromised as a result
of interbreeding. Interbreeding and gene flow between adjacent groups reduce the
potency of group selection within species because they reduce genetic differences
between adjacent populations (Hamilton 1964, 1975; Alexander and Borgia 1978).
Group selection of the sort just posited ultimately will result in individuals that
sacrifice their genetic reproduction for the good of the group because differential
extinction and/or reproduction of alleles at the group level exceeds in importance
that at the individual level. This is an effect postulated by Wynne-Edwards (1962,
1986) to explain what many ecologists saw a few decades ago as ‘intrinsic’ popula-
tion regulation that adaptively avoids over-use of the environment. It has been
invoked in ways implying that there are no special difficulties in the postulated
sacrifices. Many people believe (erroneously) that this kind of ‘genetic altruism’
(Alexander 1974, 1979, 1987) would necessarily typify a species, human or oth-
erwise, that had evolved through a process significantly involving group selec-
tion. Only a predominance of this kind of selection, it would seem, could prime
the individuals of a species to participate readily in the kind of ‘greatest good to
 Evolution of Human Intelligence } 253

the greatest number’ utilitarianism proposed by many social philosophers. The

required kind of sacrifice of one’s reproduction, however, is not expected to have
evolved, and no natural cases of this kind of selection have been documented or
are widely suspected.
2. Selection with Confluences of Interest at Individual and Group Levels.
In this kind of situation the individual who gives his life for the group (all or
any part of the population) gains genetically from the act because his indi-
vidual interests are identical with those of the group. Identity of evolution-
ary interests will be temporary in sexually recombining organisms because
individuals in such species will for the most part be genetically unique.
Identity of interests, on the other hand, is permanent in clones (barring
mutation). Altruism between genetically non-identical individuals can thus
evolve when neighbours (interactants) are alike genetically—compared to
more distant conspecifics (as in Hamilton’s (1975) ‘viscous population’—cf.
Nunney (1985))—to a degree that over-compensates the increased competi-
tiveness for resources likely to result from proximity.
Even when individual and group interests are identical, presence and prevalence
of alleles are likely to be more affected by lower levels of selection because of the
greater potency of selection there (Williams 1966; Lewontin 1970; Dawkins 1976;
Alexander 1979). Such selection would, however, be enhanced by selection in the
same direction at group levels. In sexually reproducing organisms, such as humans,
confluences of interest within groups are likely to occur when different groups are
in more or less direct competition. As a result, the kind of selection alluded to here
would be expected to produce individuals that would cooperate intensively and
complexly within groups but show strong and even extreme aggressiveness between
groups. Such tendencies characterize modern humans and chimpanzees, and there
are no convincing reasons for believing that they did not characterize humans
throughout their evolution. The kinds of inter-group interactions that occur among
modern humans and chimpanzees probably occurred throughout the evolution of
the great apes and hominids. In humans, especially, the impression of group selec-
tion can be given because of costs imposed socially for failures to be altruistic.
One reason why humans have been described as a good model for within-species
evolution by group selection is that opposing groups often behave toward one another
as if they were different species. Social rules, morality, law, and a great deal of cul-
ture represent the imposition of costs and benefits on the actions of individuals and
subgroups designed to force a convergence of their interests with those of the social
group as a whole, thus tending to create the second kind of situation described above.
It seems to me that, after more than 50 years of discussion and analysis, the
appropriate conclusion from all the arguments on the topic of self-sacrifice, hero-
ism, and altruism toward others is still that suggested by Fisher (1930: 265): ‘The
mere fact that the prosperity of the group is at stake makes the sacrifice of individ-
ual lives occasionally advantageous, though this, I believe, is a minor consideration
compared with the enormous advantage conferred by the prestige of the hero upon
254 { Human Social Evolution

all his kinsmen’. Even the extreme cases of Japanese kamikaze pilots in World War II,
in which all of the men in sizeable units volunteered willingly, and even insistently
and competitively (Morris 1975)—if they are to be queried in evolutionary adaptive
terms—must be analysed in the light of ceremonies, honours, and other described
effects having to do with relatives of the volunteers, and connected to the costs of
cowardice and rewards for heroism, during the long-term cultural history of Japan.

A NOTE ON COMPETITION

Humans live in groups, and individual interests are expressed in cooperation and
competition at all levels of social organization. I interpret human social organi-
zation of virtually all kinds to be cooperation, either for the explicit purpose of
direct competition with other humans also living in groups or as a part of the
indirect competition of non-intentional or non-interactive differential reproduc-
tion. With respect to the general process of evolution, the concept of competition
must be taken in this broad sense, in which it stands alone, with no real or exist-
ing opposite. Thus, cooperation, and all parallel activities, cannot be regarded
as alternatives to competition; as such they could not evolve. Cooperation must
exist because it has aided reproductive competition, however indirectly. One
individual or group can be said either to compete or cooperate with another; but
the cooperation, if it depends on evolved tendencies, also represents either direct
or indirect competition with still other such units. In evolution, only genetic
altruism (Alexander 1974, 1979, 1987) could be regarded as opposing competi-
tion, and for this reason such altruism will not evolve and will not be maintained
if it appears incidentally.

DISTINCTIVE ASPECTS OF SELECTION ON HUMANS

The nature and all-inclusiveness of organic evolution requires us to assume that
the human psyche evolved as a vehicle serving the genetic or reproductive interests
of its individual possessors. These interests are expressed in individual humans via
success in (1) survival and social integration across juvenile (and adult) life; (2)
mate-seeking and -holding as an adult; (3) offspring-production and -tending; (4)
beneficence (and the seeking of beneficence) with respect to collateral kin; and (5)
various forms of (direct and indirect) social reciprocity to both kin and non-kin
(or close and distant kin), which means beneficence dispensed in situations in
which returns with interest are expected (Trivers 1971, 1985; Axelrod and Hamilton
1981; Alexander 1979, 1987).

WHY LIVE IN GROUPS?

To understand any group-living species, such as humans, we must first ask why
organisms live in groups and then ask, in turn, why humans live in groups. I have
 Evolution of Human Intelligence } 255

previously discussed these two questions in detail (Alexander 1974, 1979: 58–65;
1987: 79–81). Partly because the above view of natural selection is fairly new in
biology, the answers are not the same as those that have been prevalent in anthro-
pology and the other social sciences.
Sociality by definition can exist only in organisms that live in groups. Efforts
to understand sociality for a long time rested upon the intuitive view that groups
exist for the good of the species, and individuals for the good of the group. If
selection is more potent at individual than at group levels, however (see above),
we should expect organisms to behave as if their own reproductive success is what
matters (and they do—see examples in Alexander 1979, 1987).
Except in clones, the life interests of individuals within groups are rarely iden-
tical. If behaviour evolves because it helps its individual possessors, then group-
living inevitably entails expenses to individuals, such as increased competition for
all resources, including mates, and increased likelihood of disease and parasite
transmission. Why, then, should animals live in groups? Why be social, beyond
the minimum required to mate and raise a family (indeed, why even keep one’s off-
spring near for a time)? If the answer is that individuals living in groups reproduce
more than individuals not living in groups, what are the reasons?
Theoretically, the causes of group-living include enhanced access to some
resource, or enhanced ability to exploit a resource, which more than offsets,
for individuals, the automatic detriments. I have previously argued (Alexander
1974) that reasons for group-living are few in number:
(1) lowering of susceptibility to predation either because of aggressive
group defence or because of what Hamilton (1971) called selfish herd effects
(e.g. a more effective predator detection system or the opportunity to place
another individual between one’s self and a predator); (2) cooperative secur-
ing of fast, elusive, aggressive, or hard-to-locate prey; and (3) localization of
resources (food, safe sleeping sites, etc.) that simply forces otherwise solely
competitive individuals to remain in close proximity (see also Alexander
1975, 1979).
It is obviously useful to distinguish, when possible, between the primary causes
of group-living and its secondary results. Postulated causes of group-living other
than those listed above are probably secondary. For example, it seems unlikely that
cooperative defence of clumped resources could ever be a primary cause of group
living, since clumping of resources would at first yield the third kind of group-
living just listed (Alexander 1974). My own opinion is that groups, such as in pri-
mates, that cooperate now, whether to defend food, females, or territory, probably
evolved originally because of predator influence (even if what was at first involved
was only one or a small group of females protecting their young) and secondarily
(after having evolved cooperative tendencies or abilities in other contexts) began
to defend food resources in those groups. Similarly, I would suppose that defence
of large prey items in cooperatively hunting canines and felines is also secondary,
256 { Human Social Evolution

evolving after group hunting. Again, group hunting most likely took the initial
form of one or two parents hunting with their own offspring. It is obviously easier
to understand cooperative interactions within groups of relatives, especially par-
ents and offspring, than among nonrelatives.
Wrangham (1980), Cheney and Wrangham (1987), and others have downplayed
the role of predation in causing group-living in primates, mainly because of the
paucity of observations of predation. Nevertheless, predation is probably respon-
sible for herding in ungulates and colonial life in a great many vertebrates that live
in groups similar to the groups of related females discussed in various primates
by Wrangham (1980), and that have little possibility of being explained as defend-
ers of food bonanzas or any other resources. Moreover, Cheney and Wrangham
(1987) list estimated predation rates on 30 primate species as averaging about 6.5%
per annum.
Humans have affected predators negatively by their own actions more than prey
species, and as well may deter predators completely by their presence as observ-
ers, so the above figures can scarcely be regarded as insignificant. Indeed, the only
other significant source of primate mortality discussed in Smuts et al. (1987), is
infanticide by conspecifics. Predation is also rarely observed in many species
where the observers do not doubt that it has been responsible for chemicals, pow-
erful senses, mimicry, cryptic coloration, or the patterning of social life or group
living (e.g. Alcock 1984). If one wishes to answer the question of why groups form
and persist, moreover, observed rates of predation on normally structured social
groups are far less significant than observations of the fates of individuals outside
their social groups, or in groups that, for example, lack large males or are abnor-
mally small.

CAUSES OF HUMAN GROUPING

Early groups of humans are widely believed to have been group hunters. This idea
is not incompatible with evidence that gathered foods provided most of the diet
of early humans (e.g. Lee 1968; Tooby and DeVore 1987); but gathering seems less
likely to have led to complex cooperative tendencies (for perhaps the best case for
the alternative possibility, see Kurland and Beckerman 1985). If arguments given
earlier are correct, the predecessors of the earliest hominid group hunters almost
certainly lived in groups because, as with probably all modern group-living non-
human primates, they were the hunted rather than the hunters. By all indications,
humans are the only primate that became to some significant extent a group-
hunter—the only group-living primate who, at least for a time, has escaped having
its social organization essentially determined by large predators (chimpanzees are
nearest to being an exception in both regards, but they obtain far less meat from
hunting, and they are obviously subject to human and other kinds of predation:
see King 1976; Goodall 1986; Cheney and Wrangham 1987). For this reason it is not
surprising that we empathize to some degree with canine and feline social groups.
 Evolution of Human Intelligence } 257

The human brand of sociality appears to have been approached by various other
primates because they are our closest genetic relatives, but by canines and felines
(lions) because they most nearly (among nonprimates) do, socially, what we did
for some long time.
But the organization and maintenance of recent and large human social groups
cannot be explained by a group-hunting (or gathering) hypothesis (Alexander
1974, 1979). The reason is that the upper size of a group in which each individ-
ual gained because of the group’s ability to locate and secure large game or other
food bonanzas would be rather small. Indeed, according to such a hypothesis, as
weapons, skills, and cooperative strategies improved, group sizes should have gone
down, owing to the expenses (to individuals) of group-living, which tend to be
exacerbated as group sizes increase (acceptance of this argument depends on the
assumption of powerful selection below the group level). Cooperative group hunt-
ers among nonhumans tend to live in small groups (canines, felines, cetaceans,
some fish, and pelicans); and most large groups (e.g. herds of ungulates) are prob-
ably what Hamilton (1971) called ‘selfish herds’, whose evolutionary raison d’être is
security from predation. (The relevant security is to individuals, but not necessar-
ily to the species as a whole; as Hamilton pointed out, the population can actually
suffer higher overall predation, but because existence of groups causes predation
on lone individuals to become even more severe, group-living in selfish herds
can nevertheless continue to evolve.) Even groups evidently evolved to cooperate
against predators are typically small (chimpanzees, baboons, musk ox). But maxi-
mum human group sizes, beginning at times and places not easily ascertainable,
went up—right up, eventually, to nations of hundreds of millions.
Modern human groups are unique, suggesting that explaining them will call for
selective situations that are in some sense unique. Thus, other complexly coopera-
tive groups either tend to be small, as with cooperatively hunting groups of canines
or felines, or else they are structurally unlike human groups. In human groups, for
example, coalitions exist at many levels of stratification, and in many functional
contexts. Clones are often very large, as are modern human groups, but clones are
composed of individuals with continuously identical evolutionary interests, while
human groups are not. Eusocial insect colonies, such as those of ants and termites,
are often both huge (up to 15–20 million: Wilson 1971) and complexly social, as
with humans. But they represent variations on a nuclear family theme. In them,
a single female (usually) and one or a few males produce all the offspring, and
all but these few reproductive individuals tend to be full or half siblings to one
another. Even in a eusocial colony of millions, every individual is closely related
to every other one. Completely unlike this, large human groups are composed
of close and distant relatives, and nonrelatives; and every individual expects to
reproduce unless special circumstances intervene. Moreover, in the huge modern
eusocial insect colonies, such as with ants and termites, the interests of the differ-
ent colony members, whether queen or workers, may be virtually identical. The
reason is that all will realise reproductive success only through the rather small
258 { Human Social Evolution

group of reproductively mature individuals that will emigrate and found new colo-
nies. Not only are the workers and the queen likely to be similarly related to these
reproductives (especially in forms with diplo-diploid sex determination, as with
termites), but they are likely to have no other opportunity to reproduce. A good
comparison in familiar terms would be represented by a species in which the male
and female tend to be obligately monogamous, bonded for life. If opportunities for
differential assistance to nondescendant relatives, and for philandering, are rare
or non-existent, then, even though the male and female may be completely unre-
lated, their reproductive interests are identical. Each will reproduce only via the
offspring they produce together; and in most cases the two parents will be equally
related to the offspring. In such cases the male and female are expected to behave
as though their evolutionary interests are identical, as with members of clones, and
queen and workers in some eusocial colonies (Alexander 1987).
In this light, conflicts of interest take on special significance in the huge modern
social groups of humans: such conflicts are more or less continual, and they can
become exceedingly complicated. They wax and wane in response to competitive
and cooperative interactions of groups with one another, as well as in response to the
interactions of individuals within groups. As we shall see, chimpanzees live in multi-
male groups that in some ways parallel those of humans, and this is significant for
efforts to understand human evolution and the nature of the human psyche.
In trying to explain how modern humans developed such huge and unified politi-
cal groups, and became involved in the current international arms race, it is possible to
argue that the early benefits of group-living—whatever they might have been—were
so powerful that they produced humans with such strong tendencies to be socially
cooperative that the huge groups of recent history developed as more or less inciden-
tal effects, despite wide-spread deleterious effects on the reproduction of the individu-
als that comprised them. Such a view may at first seem correct, in the sense that living
in small, highly cooperative groups may have produced humans who readily adopt
competitive or adversarial attitudes toward members of other groups, and continually
compare the relative strengths of groups and strive to produce or maintain strength
(through extension and intensification of cooperation) in their own group (Hamilton
1975). But this view allows continual readjustments that return positive effects on the
reproduction of individuals living in groups. In any other sense, the argument implies
a degree of rigidity, or a kind of genetic control, of behaviour that I would like to
regard as an argument of last resort. Moreover, if this latter kind of rigidity were the
correct view, then we should not be able to identify widespread advantages from liv-
ing in large groups currently, and alternative hypotheses to explain modern human
groups should be difficult to apply. Neither is the case.

IMBALANCES OF POWER AND RUNAWAY SOCIAL COMPETITION

The general hypothesis that I support to account for the maintenance and
elaboration of group-living and complex sociality in humans, described earlier,
 Evolution of Human Intelligence } 259

derives from a theme attributable to Darwin (1871) and Keith (1949), and developed
by a succession of more recent authors (Bigelow 1969; Carneiro 1970; Wilson 1973;
Pitt 1978; Strate 1982; Betzig 1986; Alexander 1967–1988; Alexander and Noonan
1979; Alexander and Tinkle 1968). It includes group-against-group, within-species
competition as a central driving force, leading to balance-of-power races with a
positive feedback upon cooperative abilities and social complexity. It implies that
the only plausible way to account for the striking departure of humans from their
predecessors and all other species with respect to mental and social attributes is to
assume that humans uniquely became their own principal hostile force of nature.
This proposition is immediately satisfying, for it (perhaps alone) can explain
any size or complexity of group (as parts of balance-of-power races). It accords
with all of recorded human history. It is consistent with the fact that humans
alone play competitively group-against-group (and, indeed, they do this on a large
and complex scale)—if play is seen, broadly, as practice. And it accords with the
ecological dominance of the human species and the disappearance of all its close
relatives.
No other sexual organisms compete in groups as extensively, fluidly, and
inexorably as do humans. In no other species, so far as we know, do social groups
have as their main jeopardy other social groups in the same species—hence, the
unending selective race toward greater social complexity, intelligence, and clever-
ness in dealing with one another at every social level. No other species deals in
war so as to make it a centre-piece of social cooperation and competition. I am not
aware of hypotheses other than that given above which can deal with all of these
issues.
Most of the evolution of human social life, I am hypothesizing, and the evolution
of the human psyche, has occurred in the context of within- and between-group
competition, within-group competition shaped by between-group competition,
and the centrality of social competition resulting from the ecological dominance
of the human species. Once cooperation among individuals (and subgroups)
became the central means of within-species competition, the race toward intel-
lectual complexity was on. Without the pressure of between-group competition,
within-group competition would have been relatively mild, or at least dramatically
different, because groups would have remained small and would have required less
unity and different kinds of cooperativeness. There would have been no selective
pressure that could produce the modern human intellect.
The situation I am postulating is not simply that described by Darwin’s obser-
vation that, because of their similarity to one another, the members of a species
are their own worst competitors for food, shelter, mates, and so forth. Rather, this
view calls for a species that has so dominated its environment that all other hostile
forces have been manipulated and modified into relative trivialities, compared to
the effects of competitive and cooperative conspecific neighbours. If there are forces
that remain potent (for humans, parasites are the most obvious example), then
my argument would suggest that they could not be neutralized effectively by
260 { Human Social Evolution

human effort in ways that led to major long-term trends in behaviour that could
account for the evolution of the human intellect (the reasons might be erratic or
infrequent appearance, rapid evolution, invisibility, or other causation that has
somehow been outside human knowledge or capabilities of thwarting). In present
circumstances the AIDS virus, a ‘social’ disease, might be seen as a counterex-
ample to my argument. It seems beyond doubt that this disease is at least tem-
porarily modifying human sexual and social behaviour in a significant fashion.
Particularly interesting is the extent to which people who previously regarded as
immoral actions that increase the likelihood of contracting AIDS use this jeop-
ardy to promote their particular views of morality. To place AIDS-like diseases in
an appropriate perspective with regards to human evolution, however, one has to
consider what the reaction to them would have been without modern technology
and knowledge from it. It seems unlikely that connections would be easily estab-
lished between sexual interactions and physical deterioration many years later, or
that sexual behaviour would have been severely modified prior to modern medical
knowledge.
Runaway social competition can be understood by considering three features:
(1) interminable conflicts of interest that cause social competition to be unending;
(2) runaway aspects that can come into play most powerfully when the competi-
tion is within species; and (3) minimizing of brakes or direction changes because
of the ecological dominance of the human species.
Interminable conflicts of interest cause unending evolutionary races. Such races
occur, for example, between predators and their prey, so long as two species remain
in this relationship to one another. They also occur within species, as between
males and females, when conflicts of interest exist between the sexes in regard to
the social interactions that sexual reproduction requires them to undertake. For
example, males in many insect species use their genitalia in ways contrary to the
interests of females, such as by holding the female longer than is to her advantage
during copulation, so as to decrease the likelihood of another copulation and com-
petition from the sperm of another male. Females may be expected to evolve to
extricate themselves sooner, males to evolve to hold them more effectively; and the
race is potentially unending. Similarly, in many mammals, males can maximize
their reproduction only by mating with multiple females and showing little or no
paternal care, while females in the same species can only maximize their repro-
duction by securing more paternal care than is advantageous for males to give.
Such conflicts can lead to rapid evolutionary change, and sometimes unending
races, in which each party evolves in response to the particular changes that occur
in the other: what is beneficial for a male will depend on what countering changes
occur in females, and vice versa (although extrinsic environmental changes may
also be crucial in both of these examples).
One of the relevant facts from the ‘balance (or imbalance) of power’ argu-
ment described above for humans is that in social-intellectual-physical competi-
tion (such as physical competitions in which intelligence and the ability to gain
 Evolution of Human Intelligence } 261

and use support from others are important), conspecifics are likely to be—as no
other competitors or hostile forces can be—inevitably no more than a step behind
or ahead in any evolving system of strategies and capabilities. (The exception is
when geography restricts contact, hence prevents more or less continual transfers
of information via either aggression or cooperation and allows either cultural or
genetic divergence or both.) Evolutionary unending races are thus set in motion
that, because of the presumed paucity or absence of hostile influences extrinsic to
the human species, have a severity and centrality as in no other circumstance. In
other words, human social competition may be expected to involve a ‘runaway’
aspect, comparable to Fisher’s runaway sexual selection, that is not likely in evo-
lutionary races between, say, predators and prey. Indeed, the postulated process
could be more extreme than runaway sexual selection.
Fisher (1930: 58) used the term ‘runaway’ sexual selection for situations in
which females (usually) begin to favour extremeness of traits in males, leading
to greater mating success by males that possess extremes of traits that are del-
eterious in every other respect (Trivers 1972). Within-species social competition
is likely to take on ‘runaway’ aspects for three reasons: (1) the interdependence
of the adversarial parties causes the significance of change in one to depend on
the traits of the other; (2) the traits involved in the competition are likely to be
arbitrary (and deleterious) in all other contexts; and (3) within-species groups of
an ecologically dominant species such as humans are relatively immune to effects
from other selective agents. When one’s adversary continually remains similar or
identical to one’s self in all but the particular trait that is at the moment changing,
when changes in one party depend solely upon changes in the other, and when
other hostile forces are insignificant, then there are few or no brakes on change in
the traits used in the competition, and little extrinsic guidance (cf. West Eberhard
1979, 1983). I believe that the current human arms race is the prime example of
such a process, and as well a logical outcome of the history that such a process
suggests for the human species (Alexander 1987).
Runaway social competition would (perhaps alone) account for the fact,
stressed earlier, that human evolution has resulted in a single species, with all the
intermediate forms having become extinct along the way. (I also speculate that the
evolving human line has for a long time been a severe predator and competitor of
apes, and is at least partly responsible for the low number of surviving Pongidae.)
Indeed, unlike any other hypothesis so far advanced, it appears to require this out-
come. It could also account not only for an acceleration of the relevant changes
in the psyche, in social organization, and in culture in general, at certain stages
of human social evolution, but as well for deceleration or even reversal of the
direction of evolution of the psyche at other stages (Alexander 1971; Pitt 1978).
Stringer (1984) summarizes the evidence that ‘ . . . the autocatalytic model of endo-
cranial volume increase seems most appropriate since there is an increasing rate
of change until the late Pleistocene, when endocranial capacity values stabilize or
even decline’. All that is required for the presumed stabilization or decline is that
262 { Human Social Evolution

(1) social change eventually creates large societies in which the kinds of abilities
and actions that preserve the entire group are possessed and used appropriately
by smaller proportions of the society’s members (in their own interests); and (2)
group success and the social structure somehow lessen the reproductive disad-
vantages previously suffered within (and between) societies by those who lack the
qualities of such leaders or governors. As numbers of leaders diminish in rela-
tion to numbers of followers—with increases in the sizes of social and political
groups—the probability of producing a sufficient number of individuals with the
necessary qualities to lead or govern effectively (whatever these qualities may be)
would not necessarily diminish, owing partly to effects of genetic recombination.
This condition (absence of advantage for increased complexity of mental activity)
may exist in all large societies today (e.g. Vining 1986; compare with Alexander
1988). Whether or not it accounts for what Stringer describes (which could also
reflect changes in brain structure consistent with the previous trend towards
greater brain size, body size changes, or other forces) is another question.
In human intergroup competition and aggression, there are two prominent
facilitators that unbalance the power of competitive groups, leading to more dra-
matic outcomes of confrontations and a greater likelihood of significant group
selection in the form of unilateral extinction or one group taking over another’s
women and resources (Alexander 1971). These are (1) social and cooperative abili-
ties that allow or cause larger (hence, variable) group sizes, and more concerted
and effective group actions; and (2) culture and technology, which can provide
one side or the other with superior competitive ability through means as diverse as
language, weapons, and patriotic or religious fervour or perseverance. Changes in
these regards can repeatedly adjust balances of power and fuel the kind of runaway
social competition here postulated.
This argument may be compared to Gowlett’s (1984) comment that ‘It has become
widely accepted that . . . biological evolution and cultural evolution affect one another
in a positive feedback relationship, thus providing both change and its cause’.

‘INITIAL KICKS’ OR WHAT STARTED THE PROCESS?

As Wilson (1975: 568) notes: ‘Although internally consistent, the autocatalysis

model contains a curious omission—the triggering device.’ Gowlett (1984) also
argues that any such view as the above ‘ . . . accounts for a process that is going on,
rather than for the start of it. It does not satisfy the desire for a single perceptible
factor, an “initial kick” which starts off human evolution. Consequently hypothesis
after hypothesis has emerged in which such a kick has been found, and in some
of them its momentum dominates the whole story.’ In other words, even if the
above scenario were acceptable, it is still essential to know how, when, and why
the ancestors of modern humans became involved in an evolutionary, balance-of-
power, runaway social competition.
 Evolution of Human Intelligence } 263

In chimpanzees and a few other primates that live in multi-male groups—as in

humans—females rather than males move between groups (Wrangham 1979; Pusey
and Packer 1987; Cheney 1987). This change allowed males to bond, in connection
with defending the home area as bands of relatives. Cheney (1987) and Manson and
Wrangham (n.d.) believe that the initial resource involved in intergroup aggression
was females; and they cite chimpanzees as most like us in these regards. King (1976)
regards the pivotal resource as territory, but the point is the same: male coopera-
tiveness and territoriality, coupled with female transfer, lead to intergroup aggres-
sion. Following King, Manson and Wrangham also lay great stress on variability in
sizes of attacking and attacked groups, which they say is likely in human hunter-
gatherers and chimpanzees partly because they live in ‘communities’, in which (as
Reynolds 1965, pointed out) ‘travelling parties are almost always subgroups of the
politically autonomous unit’. Wilson (1975) speaks of ‘the fluidity of chimpanzee
social organization’ being ‘truly exceptional’. King refers to this fluidity as tempo-
rary fragmenting of otherwise stable societies, while Manson and Wrangham use
Kummer’s (1971) phrase ‘fission and fusion’. In other words, through temporary alli-
ances with individuals and subgroups with whom relationships have been main-
tained in the larger ‘community’, chimpanzees—as with humans on an immensely
larger scale—meet threats, some of which are posed by other cooperating groups of
conspecifics (Goodall 1986; Manson and Wrangham, n.d.).
Chimpanzees are evidently also most like humans psychically, using as criteria
their performances at linguistic and other tasks in the laboratory, their use of tools,
their tendencies to hunt cooperatively and to cooperate against ‘enemies’, and the
evidence that they possess a self-awareness in some sense paralleling our own
(which, however, at least orangutans share—Gallup 1970; Suarez and Gallup 1981;
see also Premack and Woodruff 1978). Manson and Wrangham (pers. comm.) are
sceptical that the cognitive abilities shared by humans and chimpanzees are rel-
evant to the conduct of intergroup aggression. On the other hand, cooperation,
coordination of emotions by displays, bluffing, and anticipation (if not planning)
all seem to occur in connection with chimpanzee attacks on members of other
groups (references in Goodall 1986; Smuts et al. 1987). My view is that the evidence
for (1) cooperation to compete against conspecifics and (2) social reciprocity, fore-
sight, and deception in both chimpanzees and humans implies that this combina-
tion of attributes has functional significance.
In general, the above arguments are compatible with the scenario developed
here and earlier for the driving forces in human evolution (Alexander 1967–1988;
Ghiglieri 1987, 1988). They help clarify the similarity between humans and chim-
panzees, and that similarity implies that the processes suggested here were initi-
ated quite early, before the primates involved would have been termed ‘human’ by
modern investigators (see also Wrangham 1987).
These arguments tend to support an affirmative answer to Gowlett’s (1984)
question whether or not ‘the earliest known men were hunters’ (see also Tooby
and DeVore 1987). The question remains whether chimpanzee (and pre-human)
264 { Human Social Evolution

males initially cooperated to defend against predators, to hunt, to defend terri-

tory (or females or both), or to ‘export’ aggression to other males (Manson and
Wrangham, n.d.). My scenario has these behaviours occurring in the order just
given (Alexander 1979: 223), and suggests that, in a primate physically, socially, and
psychically like chimpanzees or ourselves, cooperative hunting or defence of territory
or females are all adequate ‘initial kicks’ for intergroup balance-of-power races if
extrinsic hostile forces are sufficiently insignificant.
All of these comparisons imply to me that if by some chance the human spe-
cies should be extinguished while chimpanzees were not, there is a fair chance
that chimpanzees would embark upon an evolutionary path paralleling in some
important regards that taken by human ancestors across the past million years
or so. Indeed, they also imply that chimpanzees have been kept in their current
status by the predatory and competitive actions of humans (Alexander 1974: 335),
and that if they were even more like humans than they are, they would have long
ago suffered the same fate that I believe had to befall the closer relatives of mod-
ern humans: extinction by their closest relatives, the evolving human line. Cheney
and Wrangham (1987) refer to humans as ‘particularly dangerous predators’, of
baboons, so classified with lions, and remark that ‘. . . human predation no doubt
accounts for the greatest number of primate deaths, even in areas where hunt-
ing methods are still primitive. The regular hunting of primates by hunter-gather-
ers suggests that humans were important predators of nonhuman primates long
before the advent of firearms and that human hunting may have exerted an influ-
ence on the evolution of antipredator behaviour and even social structure . . . ’ (see
also Tenaza and Tilson 1985). I emphasize that the scenario I am developing does
not require that the relevant competition be restricted to members of the same
species; rather, it would be expected that any species similar to a species in which
intergroup competition had become regular and intense would also be in jeopardy.
Female dispersal, and male relatives defending territory cooperatively in
both chimpanzees and humans, cause even more intrigue to be attached to the
relationship between male competition for females—both within and between
groups—and the perplexing problem of (1) the rise of despotism (including
extreme polygyny for despots) in societies of intermediate sizes and social com-
plexity (tribes, chiefdoms,), yet (2) the institution of socially-imposed monogamy,
reverence for the nuclear family, and suppression of extended families and kin
networks in still-larger human societies (nation-states) (Alexander 1979, 1987, in
press; Betzig 1986; Harpending 1986). Various authors (Levi-Strauss 1949; Irons
1981; Flinn and Low 1986) have pointed out that, in humans alone, males treat
females as commodities, to be bargained with and for, in connection with their
movement between groups. (Two major differences between chimpanzee and
human societies are that human males show paternal care, while chimpanzee
males do not; and human females conceal ovulation, thus affording males some
confidence of paternity, while chimpanzee females advertize their ovulation and
mate promiscuously—Goodall 1986; Alexander and Noonan 1979). Whether or
 Evolution of Human Intelligence } 265

not women were the resource that led to the initiation of intergroup aggression,
and even if sexual selection has remained prominent in the activities of war and
the admonitions given to young men of fighting age (Alexander 1987; Manson and
Wrangham, n.d.), it is most unlikely that women are still a central resource at issue
in the international arms races that baffle us all (see also below).
The nettlesome question, of course, is why are [chimpanzees] territorial?
Where is the survival advantage in risking one’s life for land? The answer
appears to be that winning more habitat enhances a group’s mating success.
Because ecological resources limit the number of females who can live in any
region, the success of males in expanding, or at least holding, their territory
determines the upper limit of their reproductive potential. No wonder they
are territorial; if they were pacifists, or even individualists, their more coor-
dinated neighbours would carve their territory into parcels and annex them.
Thus armies are introduced into the natural arms race. Once this happens, sol-
idarity between a community’s males becomes essential (Ghiglieri 1987: 70).

DIFFICULTIES IN ADVANCING EVOLUTIONARY UNDERSTANDING OF

OURSELVES

Evolution proposes to explain the explainers themselves. The difficulty of this

proposition lies not only in the fact that some of the traits to be explained must
be used in their own explanation, but also that one trait of the explainers is that
they do not always wish to be explained—at least not too completely to anyone
else—and that humans, more than any other species, are evolved to be exceedingly
clever at deceiving other humans. Moreover, there may be no task of learning or
teaching that is imaginably more difficult than that of bringing into the conscious
items that have been kept out, not incidentally but by natural selection, and most
particularly by selection that has disfavoured conscious knowledge of motivation
as a social strategy.
There are probably two other main reasons for the slow progress of evolution-
ary understanding, especially with respect to ourselves:
1. Applying evolution to the understanding of organisms is not easy,
even if the process itself is deceptively simple. Such understanding is dif-
ficult because organisms are exceedingly complex. It calls for understanding
the relationships between gene action and development as well as physi-
ological, morphological, and behavioural outcomes and their variations. It
is helped greatly by a repeated or continual necessity of dealing with these
problems, a difficulty that many biologists face on a daily basis while most
nonbiologists do not.
2. The preceding difficulty is exacerbated by two facts: first, most people
don’t care about evolution, believing that it has little effect on their personal
266 { Human Social Evolution

everyday lives; and, second, some people care too much. Evolutionary argu-
ments seem to many to threaten cherished beliefs about humans and their
history. Evolutionary arguments about humans also come from biology—
a field distinct from the social sciences and the humanities, and one tra-
ditionally preoccupied with nonhuman species. Moreover, evolution has
had a notoriously poor record in explaining humans in the past: during the
decades when the social sciences were developing, biologists simply did
not know how to apply selection to understand behaviour. For the most
part they didn’t even try, and so the social sciences developed more or less
independently of biology and evolutionary theory. Finally, science and the
humanities—disciplines preoccupied, respectively, with searches for unde-
niable facts and meaning or values—clash when biologically oriented scien-
tists begin to analyse human actions in terms of their functions or effects,
because such analyses seem to infringe on questions of meaning and value,
hence to represent ideologies (Alexander 1988).

Cooperation also seems always to be a matter of congeniality and pleasantness.

The concept of competition, and the idea of evolution by natural selection, on the
other hand, imply nastiness. As already noted, however, in evolutionary terms
cooperation and competition are not opposites, but rather, cooperation is necessar-
ily a form of competition, which can be either indirect and remote, or quite direct.
We have evidently evolved tendencies to develop proximate feelings that make it
convenient to ignore the competitive effects of cooperative activities that give plea-
sure to us and our associates. It is also widely believed that group selection implies
peaceful and non-competitive existence, as compared to selection at lower levels. As
the definitions and descriptions of group selection given earlier indicate, this is not
necessarily so: group selection and its mimics, as with some of the most pleasurable
and intimate forms of cooperation, can also imply the most heinous and destruc-
tive kinds of between-group competitive interactions. The vilest of discriminatory
jokes can be told in an atmosphere of warmth and conviviality; and, as Bigelow
(1969) noted, ‘A hydrogen bomb is an example of mankind’s enormous capacity
for friendly cooperation’. He suggested, with irony, that its successful construction
might seem an occasion for us to ‘pause and savor the glow of self-congratulation
we deserve for belonging to such an intelligent and sociable species’.
Only with such considerations in mind, I think, is there likelihood of a thorough
understanding of the human psyche, or other distinctive human features. Even if it
seems inappropriate to emphasize the competitive and not-so-honourable sides of
human action, motivation, and history, neither is it helpful to dismiss summarily
the possibility of distasteful kinds or intensities of reproductive competition from
human history as over-simplifications or reductionisms not deserving of consid-
eration as causative forces in determining our present psychological makeup and
socio-cultural forms.
 Evolution of Human Intelligence } 267

The Nature Of The Human Psyche

There have been few efforts to characterize the human psyche in terms use-
ful to those who would understand and reconstruct its functional aspects from
a modern evolutionary viewpoint (but see Premack and Woodruff 1978; Griffin
1978; Savage-Rumbaugh et al. 1978, and the accompanying commentaries). I think
the key argument (Humphrey 1976, 1978, 1983; Alexander 1979, 1987) is that con-
sciousness represents a system of (1) building scenarios or constructing possible
(imagined) alternatives; (2) testing and adjusting them according to different pro-
jected circumstances; and (3) eventually using them according to whatever cir-
cumstances actually arise. Earlier, I referred to such abilities as the capacity to
over-ride immediate rewards and punishments in the interests of securing greater
rewards visualized in the future (Alexander 1987). In this view, consciousness, cog-
nition, and related attributes—which probably represent the core of the problem
in understanding the human psyche—have their value in social matters, and the
operation of consciousness can be compared to the planning that takes place in
a game in which the moves of the other players cannot be known with certainty
ahead of time. In other words, by this hypothesis, the function of consciousness
is to provide a uniquely effective foresight, originally functional (sensu Williams
1966) in social matters, but obviously useful, eventually, in all manner of life cir-
cumstances. I will argue (below) that the emotions, linguistic ability, and personal-
ity traits are primarily communicative devices, hence, also social in their function.
The above view of the psyche is compatible with that of cognitive psychologists,
such as Neisser (1976). Cognitive psychologists, however, concentrate more on
mechanisms than on function, and so the idea that the use of cognition might have
evolved explicitly in the context of social competition seems not to have emerged
in their arguments. Nevertheless, Neisser’s insistence on use of the concept of
‘schemata’ as plans, representing what is here called scenario-building, is a close
parallel to Humphrey’s arguments and my own. It is clear that a merging of ideas
is likely to be easy, and profitable.

FUNCTIONS OF THE PSYCHE

Learning would appear to include two forms: (1) accumulating memory banks;
and (2) modifying memory banks, when ‘memory bank’ means a store of infor-
mation that influences abilities and tendencies to act. In some sense all pheno-
types are memory banks, in which some (genetic) information carried over from
the previous generation (and, to a decreasing extent, from increasingly distant
ancestors) has been ‘interpreted’ (‘read out’) by the environment of the phenotype
(organism), including its associates (e.g. parents) as a result of what is commonly
called epigenesis, or ontogenetic or experiential plasticity.
Humour and Play. One can learn (1) by trial and error or successive approxi-
mation of the actual performance that is useful or desired, or of surrogates of it
268 { Human Social Evolution

(practice? play?); (2) by observing and then imitating or avoiding; or (3) by being
told about (taught) or by thinking about (and imitating or avoiding). The last two
methods, at least, imply ‘observing in the mind’. Learning by observing in the
mind parallels the concept of play as practice. Play can be solitary-physical (as
with a cat practising predation by playing with a twig or a bunch of dry grass);
social-physical (as in practice-fighting or play-fighting); or social-intellectual (i.e.,
without a prominent physical component, as with building of social scenarios
through thinking, dreaming, planning, humour, art, or theatre). Presumably, there
are also intellectual (or mental) components to both solitary-physical and social-
physical play (e.g. for the latter, in team sports involving complex strategies, bluff,
and deception or trickery).
I agree with Fagen (1981) in regarding the concept of practice (including low-
cost testing) as representing the best general theory of play, and I so use the con-
cept of play throughout this paper (for a best-case dissenting argument, see Martin
and Caro (1985) who note that ‘at present, there is no direct evidence that play
has any important benefits, with the possible exception of some immediate effects
on children’s behavior’). Fagen concludes (p. 388) that ‘Current understanding
of the functions of animal play suggests that individuals play in order to obtain
physical training, to train cognitive strategies, and to develop social relationships’.
He also reviews an extensive literature attempting to connect play behaviour to
human deception, self-deception, dance, music, literature, painting, and sculpture
(pp. 467 ff.; see also Wilson 1975). He describes ‘hints at essential relationships
between play and creative thought’ in the words of Einstein and the thoughts of
some other scientists, noting that ‘these unsatisfactory metaphors are the best
currently available links between play and human creation’. Klopfer’s (1970) brief
comment probably comes closest to the discussion of social-intellectual play
developed here. Describing aesthetics as ‘the pleasure resulting from biologically
appropriate activity’ and play as ‘the tentative explorations by which the organism
“tests” different proprioceptive patterns for their goodness of fit’, Klopfer suggested
that ‘thought and abstraction in man is but a form of play’ and ‘Abstractions may
be the play through which we learn how to think well’ (Klopfer 1970: 402–403).
To Fagen’s conclusions (above), I would add that play sometimes represents low
cost repetitions and out-of-context or pretend ‘run-throughs’ in the interests of (1)
practising for predictable situations that cannot actually be experienced before-
hand; (2) preparing for different preconceived alternatives in unpredictable situ-
ations; and (3) assessing skills and abilities of one’s self and others. As Humphrey
(1986) says, ‘ . . . play is a way of experimenting with possible feelings and possible
identities without risking the real biological or social consequences’. It is also obvi-
ous that playing individuals can learn about one another and establish (accept)
dominance relationships in low cost situations which may persist into high- cost
situations; conversely, they may also learn how to reverse such relations in their
own interests. Symons (1978b; pers. comm.) argues that ‘dominance rankings are
very unlikely to be established during play’. But I know from personal experience
 Evolution of Human Intelligence } 269

that, at least in humans, they can be either established or altered during play; and
that play may be entered into with such goals explicitly in mind. I have done both,
and I suspect that few humans do not share this experience.
Loizos (1967) exemplifies the authors who present objections to the general the-
ory that play is practice (see also Martin and Caro 1985; for arguments very similar
to mine, see Fagen 1982; Symons 1978a). One of Loizos’ objections distinguishes
play from practice: ‘ . . . it is not necessary to play in order to practise—there is no
reason why the animal should not just practise”. But I regard play as a form of
practice, and so believe that the mistake is precisely the other way around; a play-
ing animal is ‘just practising’. Second, Loizos, and Martin and Caro, note that not
just juveniles but also adults play. But adults also practise extensively, and there is
no reason to expect that this particular kind of practice should be absent in adults,
especially long-lived adults with complex sociality who may be subjected to new
social situations almost endlessly. Third, Loizos believes that ‘ . . . it is simply not
necessary to play in order to learn about the environment’. I would say, however,
that it is often useful to play to learn about the social environment. Loizos notes
that ‘ . . . it is inevitable that during play, or during any activity, an animal will be
gaining additional knowledge about what or who it is playing with; but if this is
the major function of play, one must wonder why the animal does not use a more
economical way of getting hold of this information’. I suggest that, with regard to
the social environment, there often is no more effective and inexpensive way of
securing information (again, Humphrey 1983: 76–79, comes closest to saying the
same thing).
Martin and Caro (1985) argue that because play ‘has only minor time and
energy costs’, is ‘highly variable and labile’, and ‘is curtailed or absent under many
naturally occurring conditions, it seems unlikely that it is essential for normal
development’. Leaving aside the conservatism of the phrase ‘essential for normal
development’, however, the low costs of play can be cited as reasons for its use
in developing social capabilities and increasing predictability of social outcomes.
Moreover, feeding is curtailed in the presence of predators and sexually recep-
tive mates, and planning is curtailed when immediate circumstances demand
attention; but this does not mean that either feeding or planning is functionless.
Any activity having its significance primarily in social behaviour is expected to
be variable. Their estimates that play uses 4–9% of a kitten’s calories (from Martin
1984) and 1–10% of total time in most species (from Fagen 1981) do not seem con-
vincing for the purpose for which they use them. Thus, one might ask what per
cent of calories and time are spent by various species in, say, the act of copulation.
Martin and Caro also question whether play should be suspected, as is com-
monly the case, of having its primary benefits later in life. They seem to disparage
the notion that juvenile life has evolved as a preparation for success in adulthood;
but there is no other raison d’être for juvenile stages (Alexander, 1990). Moreover,
benefits that occur a long time in the future are those most likely to be difficult to
identify and evaluate.
270 { Human Social Evolution

Expanding primarily from the arguments of Humphrey (1976–1986), I would

relate the evolution of the psyche, and the representational (scenario-building)
capacity of the human mind, to social play, as practice. I suggest that, during their
‘runaway’, group-against-group, social-intellectual evolution, humans went from
social-physical play (typical of all social species) eventually to social-intellectual
play (as scenario-building and practice), which probably occurs in at least rudi-
mentary forms in all complexly social mammals, and team competitions (evidently
unique, as play, in humans). Social-intellectual play I hypothesize to be practice for
later, more consequential social-intellectual (and physical) competitions (that is,
direct competition for mates or resources), just as solitary- and social-physical
play represents practice for later, more consequential solitary- and social-physical
activities or competitions (cf. Smith 1982).
I suggest that social-intellectual play led to an expanding ability and tendency
to elaborate and internalize social-intellectual-physical scenarios. Along with
the increasing elaborateness of internal scenario-building came an increasing
elaborateness of social communication, including language and the evolution of
linguistic ability. Every trait and tendency that represents or typifies the human
psyche—every mental, emotional, cognitive, communicative, or manipulative
capability of humans—I regard as a part of, derived from, or influenced by the
elaboration of social-intellectual-physical scenario-building, and of the use of
such scenarios—and of the emotions, language, and personality—to anticipate
and manipulate cause-effect relations in social cooperation and competition. This
would happen ultimately in the context of winning or losing both as an individual
within a social group and as a member of a social group, the survival of which
depends, in the end, on success in group-against-group competitions within the
species.
Just as I believe that the evident radical departure of the human psyche from
the mentalities of the closest relatives of humans can only be explained by assum-
ing that humans themselves kept driving the selection in a peculiar way, I also
believe that only other humans represent a sufficiently complex and unpredictable
force to drive the evolution of the psyche in regard to its special ability to make and
test social predictions. In other words, we became progressively better at practis-
ing for our social competitions through internal scenario-building because our
adversaries and competitors were doing precisely the same thing. And because we
all belonged to the same species, so that those with differently useful expressions
of the psyche were parts of the same interbreeding population, there has for a very
long time been a positive feedback involved in the evolution of increased human
mental capacities, with the ‘losers’ or ‘followers’ never more than a step or two
behind the ‘winners’ or ‘leaders’.
To the extent that social-intellectual play can be carried out by observing in
the mind, it can also be (1) accomplished (secondarily) in solitary (e.g. we laugh
at jokes when alone); and (2) concerned with not only social-intellectual striv-
ing or competition but also social-physical or even solitary-physical striving
 Evolution of Human Intelligence } 271

(again, secondarily: note Neisser’s (1976) relating of his ‘schema’ to locomotion).

Moreover, effects of what previously was ‘pure’ play, as practice, can begin to influ-
ence actual contests over resources; a simple example would be carry-overs, into
the resource competition of adults, of dominance rankings established during play
among juveniles. Such secondary effects ought not to confuse our identification of
primary causes.
Humans are probably not the only organisms capable of social-intellectual prac-
tice or play that does not have prominent physical concomitants. Perhaps all organ-
isms that give evidence of dreaming utilize scenario-building of some sort in their
social activities. It is easy to suspect, as Darwin (1871) did, that dogs, as well as apes
and some other primates (e.g. Humphrey 1983: 90), do these things. But it is possible
that humans alone engage in. what I see as the next stage of evolution of the intellect
in respect to scenario-building, and that is to reward or compensate others for build-
ing surrogate scenarios that are even more condensed (less time-consuming), more
elaborate (hence, more effective), and more risk-free than one’s own efforts. Once
scenario-building has become widely useful, status and livelihoods can be secured by
intellectual-social as well as other forms of occupational specialization—not merely
by taking on intellectually demanding or specialized tasks, but by using unusual
abilities and experiences to develop and conduct scenarios for others–hence, actors,
artists, musicians, writers, comedians, orators, shamans, chiefs, generals, scientists,
priests, preachers, teachers, and even professional players in sports. In this fashion,
a number of human activities, which have until now seemed inaccessible from an
approach stressing evolution or reproductive success, can be understood as a part of
explaining the reproductive significance of the human psyche.
Humour and Play. Expanding from previous arguments (Alexander 1986, 1987),
I explicitly identify humour as a form of social-intellectual play, unusual because
of its emphasis among adults, which influences resource competition directly
through status shifts. To illustrate my arguments here about the social use of intel-
lect in regard to scenario-building, humour can be seen as operating in several
different ways:

1. It can represent social practice for later competitions that will be more
direct or more expensive because they will involve the actual resources of
reproduction (jobs, money, mates, etc.). Such practice, as noted above, can
be accomplished secondarily even in solitary, just as one can practise the
moves of chess either while alone (even within one’s mind) or while playing
with others (i.e., one can laugh at a joke, and gain from the practice afforded,
even if alone).
2. It can sometimes represent the actual competition for the resources,
in the sense that the people engaging in the humour may be those with
whom one will actually compete later for significant resources; the competi-
tion may involve reputation or status that can be demonstrated so convinc-
ingly beforehand, using humour, as to turn aside expensive interactions that
272 { Human Social Evolution

would otherwise have occurred.

3. It can involve surrogate scenario-building, in which one solely or pri-
marily learns through observing scenarios built by another, such as a clown,
comedian, or writer. Such professional humourists are compensated for
building scenarios for others, more elaborately, more rapidly, or less expen-
sively than these others can do it for themselves.
4. The vicarious aspect of humour can be carried further, in the sense
that observers can alter their status among friends and associates (competi-
tors and cooperators) by the kinds of humour they exert effort to observe (or
use), and by how they respond to surrogate scenario-building via particular
forms of humour.

All of the above four uses of humour involve only its directly competitive effects
within groups. In the context of indirect competition, through within-group affili-
ation, humour can also operate in testing, promoting, or ensuring compatibility,
and willingness to cooperate, and simultaneously in establishing group limits and
thereby identifying competitors outside the group (Alexander 1986, 1987).
5. Humour can be directed against one’s self, in a version of Zahavi’s
(1975) Handicap Principle, in which the humourist demonstrates that he can
denigrate himself, or reveal embarrassing information that causes humour
in others, and still maintain superior status. As with the superior racehorse
handicapped with extra weight or the golfer handicapped with extra strokes,
both of which may still manage to win the contest, the ultimate effect can be
an enormous rise in status, worth far more than the prize for the particular
contest being waged. In these examples—and particularly in the case of self-
directed humour—even if the handicapped individual loses the immediate
contest, it can win (because of the rewards for status in human societies) in
the long run because of how well it did in spite of the handicap.
Elsewhere (Alexander 1988, n.d.) I have argued that the physical incompetence
of the human baby (its physical helplessness or altriciality), as well as that of cer-
tain other organisms, is a correlate of precociality in respect to attributes that will
improve its performance as an adult; and for humans this precociality is largely
social-intellectual. I speculate that the early and astonishing acquisition of complex
language ability in the juvenile human is related to its freedom (from the necessity of
protecting itself) to devote itself to acquiring the necessary skills and knowledge of
social communication, including practice and the analysis and acquisition of strate-
gies, in the interests of becoming a socially and intellectually more capable adult.
Observing in the mind implies consciousness and scenario-building. It also
implies being able to view and modify the memory bank with the option of saving
changes or not, as if two copies existed of the memory bank during the scenario-
building process; the question might be raised whether consciousness is somewhat
like a viewing screen (relating it, perhaps, to the concepts of short-term and long-
term memory). To observe (involve) one’s self in scenarios in the mind is, I think,
 Evolution of Human Intelligence } 273

what is called self-awareness. To practise by observing one’s self in the mind must
in some sense be a description of the source of foresight, purpose, planning, intent,
and deliberateness. Such practice gives rise to the concept of free will as freedom to
choose among alternatives visualized in the future. This view of free will contrasts
with the more widely discussed alternative implying questions about the presence,
absence, or nature of physical causation (Alexander 1979, 1987).
A parallel view, expressed in different terms, is that of Neisser (1976, especially
p. 20):

In my view, the cognitive structures crucial for vision are the anticipatory
schemata that prepare the perceiver to accept certain kinds of information
rather than others and thus control the activity of looking. Because we can
see only what we know how to look for, it is these schemata (together with
the information actually available) that determine what will be perceived.
Perception is indeed a constructive process, but what is constructed is not
a mental image appearing in consciousness where it is admired by an inner
man. At each moment the perceiver is constructing anticipations of cer-
tain kinds of information, that.enable him to accept it as it becomes avail-
able. Often he must actively explore the optic array to make it available, by
moving his eyes or his head or his body. These explorations are directed by
the anticipatory schemata, which are plans for perceptual action as well as
readinesses for particular kinds of optical structures. The outcome of the
explorations—the information picked up—modifies the original schema.
Thus modified, it directs further exploration and becomes ready for more
information.
Once planning, anticipating, ‘expecting’ organisms are interacting without
complete overlap (confluence) of interests, then each individual may be expected
to include in its repertoire of social actions special efforts to thwart the expecta-
tions of others, explicitly in ways designed to be beneficial to himself and, either
incidentally or not, costly to the others (not necessarily consciously in either case).
The expense of investing in one’s scenarios, or expectations, and of having such
scenarios thwarted, are involved in the invention of rules (see also Rawls 1971:
6; Alexander 1987: 96). Rules are aspects of indirect reciprocity (Alexander 1979,
1987) beneficial to those who propose and perpetuate them, not only because they
force others to behave in ways explicitly beneficial to the proposers and perpetu-
ators but because they also make the future more predictable so that plans can be
carried out. One of their effects, especially as the rule-makers and -enforcers come
to represent larger proportions of the group (e.g. through democratic processes),
is to converge the interests of individuals and group.
Cognition, or problem-solving ability, can, I think, easily be related to the above
arguments about the function of consciousness. Logic rationality, and cognition—
as ability to perceive cause-effect relations correctly—can be viewed in the con-
texts of dealing with either (1) social possibilities (which entails assessing probable
274 { Human Social Evolution

responses of living actors); or (2) nonsocial puzzles (some of which involve only
the somewhat more predictable logic of physical laws). The process of selecting
the most profitable (self-beneficial) among possible social alternatives involves
conscience, as ability to recognize and evaluate consequences (ultimately, repro-
ductive costs and benefits), especially as a result of the existence of rules. But in
the sense or to the extent that conscience is linked to being good or bad (moral
or immoral)—and to a failure to be conscious that one’s motivation is to serve
one’s own reproduction—either ignorance or self-deception (or both) is an obligate
concomitant. Trivers (1971, 1985) and Alexander (1979, 1987) have argued that self-
deception, via the subconscious, is a social phenomenon, evolved as a system for
deceiving others, most generally through denial of pursuit of self-interests, in turn
through denial of any broad or precise knowledge of the nature of self-interests.
I regard the emotions and their expression, as well as self-deception and per-
sonality traits, as, in the main, an extraordinarily complex system evolved in the
interests of deceiving or manipulating competitors. Deception is a crucial aspect
of competition, because only through deception can the predictable outcomes of
contests between competitors of unequal strength or resource-holding-power be
altered (Parker 1974). The possibility of deception, moreover, and the difficulty of
determining its effectiveness, can almost unimaginably complicate predictiveness
about the outcomes of contests.
Because humans are, like most other organisms, sexual reproducers, they have
evolved to behave, as individuals and families and collections of related families, as if
their life interests (which translate as genetic or reproductive interests) are unique—
different from those of other such units. Differences of interest between genetically
unique individuals may be small (as between close relatives or between spouses in
monogamy), but they do not disappear except under special circumstances, and
then only temporarily. Understanding such considerations, and the long history of
human interactions, provides the only way, I believe, for comprehending why indi-
viduals, families, social groups, and nations compete today—fiercely, continuously,
and unendingly—even when no seemingly valid or sufficient reasons are evident, or
can be given by the participants. (These arguments are expanded in Alexander 1987.)
To summarize, I have suggested that social-intellectual play, as scenario-build-
ing without extensive physical concomitants, is restricted to a small number of
intensely or complexly cooperative mammals, such as group hunters, and may
often be indicated by evidence of dreaming; in humans it is demonstrated by the
communication of representational ability. Surrogate scenario-building, or the
rewarding of others to build some of our scenarios for us, is probably restricted
to humans, as is evidently also true of rules. Morality, I have suggested, represents
the placing of more or less agreed-upon restrictions on actions that interfere too
severely with the social-intellectual scenarios and plans of other societal members,
and leads to convergence of individual and group interests.
The idea of fantasizing as play, and as problem-solving, is by no means original
here. Piaget (1945: 131) saw all imaginative thought as “interiorized play”. Symonds
 Evolution of Human Intelligence } 275

(1949), Singer (1966), and Klinger (1971) all saw fantasy as related to play and to
later problem-solving. Novel here are (1) the association of scenario-building with
social problems and deception; (2) the primacy of scenario-building as social-
intellectual practice, leading to the prominence of surrogate scenario-building in
human sociality; and (3) the argument connecting these activities to a history of
intergroup competition.

THE ULTIMATE MYSTERY: DISCREPANCIES BETWEEN THE FUNCTIONS

OF THE PSYCHE AND OUR KNOWLEDGE OF ITS FUNCTIONS

Part of the difficulty in understanding ourselves arises out of the fact that if the
human psyche is evolved to promote inclusive fitness maximizing (i.e., genetic
reproduction via both descendant and nondescendant relatives: see Hamilton 1964;
below), it clearly is not evolved to tell us precisely that this is its function and ours.
This discrepancy makes it difficult to understand what the psyche is evolved to do,
and difficult to construct a statement about what humans are evolved to do and
not to do, that makes any sense to humans themselves, in terms of their conscious
knowledge. I want to approach this problem indirectly. I am interested first in con-
structing the most general and explicit statement possible about how organisms—
eventually, and in particular, humans—are expected, from evolutionary theory, to
behave. Specifically, I wish to describe, in the most general terms, that sense in
which behaviour is evolutionarily determined, or to describe what I expect organ-
isms, because of their evolutionary history, are not able to avoid doing (Alexander
1979; 1987). In this fashion I propose to get at the question of what the human psyche
is evolved to do. The reason for interest in what organisms are not able to avoid
doing is roughly as follows: It is obvious that genes contribute to the behaviour
of organisms. They determine how particular environments affect the developing
phenotype. Equally obviously, it is not accurate to say that any particular behaviour
of any particular organism is ‘genetically determined’. The reason is that, unless
it refers explicitly to the differences between variant behaviours being genetically
determined, any such statement leaves out the effects of the environment. Thus,
if such a statement were made, outside the context of causes of behavioural varia-
tions, it is quite probable that some one could eventually identify a change in the
environment that would alter the behaviour, thus proving, in some sense, that the
statement was wrong and the behaviour was in fact not ‘genetically determined’.
Alternatively, one might say that a particular behaviour—say, how to recog-
nize or behave differentially toward kin—is learned, if he knows that particular
social experiences are necessary to cause the behaviour. But one could then ask:
Was the tendency to accept or use the learning situation in that particular way
also learned? Such questions then continue, like the turtles under the turtles in a
storied Eastern philosopher’s conception of the universe which had it ‘after that,
turtles all the way down’. But we know very well that, without some very special
definitions, it cannot be ‘learning all the way down’ because, even if they are only
276 { Human Social Evolution

potentials to action, there are genes down there, in the form, sometimes, of alter-
native alleles giving rise to potentials for different actions.

IN WHAT SENSE IS BEHAVIOUR EVOLUTIONARILY DETERMINED?

Human zygotes give rise to human organisms, honeybee zygotes to honeybees,
etc. This means that, regardless of environmental variations, particular sets of
genes produce particular phenotypes that do not vary beyond certain limits on
any axis. It is fair to say that no one expects a human zygote to give rise to anything
but a human phenotype. What is it fair to say, generally, about the limits of varia-
tion in behaviour, given a primacy for an evolutionary process guided principally
by natural selection and effective primarily at the genic or individual level, or some
other low level in the hierarchy of organization of life?
The most general statement is this: No organism is expected to act in a way con-
trary to its genetic interests, except through error or miscalculation.
To understand the significance of this statement, we must first establish pre-
cisely what are an organism’s genetic interests, so that we can recognize whether
it is doing as we expect. For example, we must understand that genetic survival is
ultimately all that counts in evolution, and that genetic survival results from repro-
duction. Success in reproduction typically involves producing more lasting copies
of one’s genetic materials than are produced by competitors and potential com-
petitors, leading to numerical preponderance, and among other things reducing
the likelihood of accidental extinction. Moreover, copies of one’s alleles appear in
collateral relatives as well as descendant relatives, and not only in offspring but in
subsequent generations as well. As a result we expect social organisms to measure
abilities of relatives available for assistance to translate assistance into increases in
reproductive success. We expect them to judge alternative ways of using life effort,
comparing their reproductive costs and benefits accurately. In short, we expect
the organism continually to be evolving to behave so as to maximize its inclusive
fitness (Hamilton 1964). Even more explicitly, we expect organisms to behave so as
to maximize, on average, the likelihood of survival of their genes—even, that is, if
some copies of their genes are in other genomes, and even if some individuals die
in the attempt because they are taking risks that are perfectly appropriate. I mean
by this that, even if a behaviour results in some copies of alleles being lost, the
behaviour may nevertheless maximize the likelihood that not all copies will be lost
(cf. Dawkins’ 1982 concept of the “extended phenotype”).
Second, we must also recognize all of the possible ways that an organism can
miscalculate, and the antecedent events that adjust its likelihood of miscalcu-
lation. For example, we must understand the concept of evolutionary novelty,
and realise that organisms may make reproductive mistakes because they have
been subjected to learning experiences or other events which alter their pheno-
types yet were not encountered by their ancestors during all the time that the
 Evolution of Human Intelligence } 277

traits and tendencies expressed today were being moulded by selection. We must
realise that competitors and predators will evolve to cause miscalculations in
their adversaries and their prey. We must understand that unpredictable events
may catch organisms in unprepared states. We must recognize that selection
against ‘errors’, especially as side effects of adaptive behaviour, can only be effec-
tive if the cost of the mistake is greater than the value of the adaptive extreme
that leads incidentally to it. We must understand that because organisms are
(evidently) selected to maximize inclusive fitness only via the accomplishment
of a wide array of more proximate ends or goals (such as avoiding pain, ingest-
ing sufficient food of the right kinds, favouring one mate over another, or risking
survival to save a brood of offspring—see below), there are innumerable ways for
inclusive-fitness-maximizing to be sidetracked. Finally, we must recognize that
we, as observers, will sometimes be able to identify actions more reproductive
than those taken by organisms, but for historical or other reasons not available
to the organism.

APPLYING THE ‘EVOLUTIONARY DETERMINISM’ QUESTION TO

HUMANS
When the problem of making a general statement about evolutionary determin-
ism is applied to humans, perplexing complications arise. Humans have what we
call an ‘awareness’ of at least some of their intentions and their purposes in life:
they can anticipate and reflect upon their activities and their goals.
If this conscious understanding about personal behaviour were tuned precisely
in the interests of inclusive-fitness-maximizing through direct and conscious
seeking of explicitly that goal, then our task would probably not be greatly com-
plicated. In such event, to make the initial statement above most meaningful for
humans, we might modify it to say: No human is expected knowingly to act in a
way contrary to its own genetic interests, except as a result of error or miscalculation.
Unfortunately, we know immediately that this is not the correct prediction
from evolutionary theory, because we know that whatever it is that humans have
brought into their consciousness, it is not a maximizing of understanding, or even
a steadily increasing understanding, of the process of inclusive-fitness-maximis-
ing. Humans are not only unaware of this process until it is explained to them, they
are instantly reluctant to believe that they are engaging in it. Even if they see some
aspects of their behaviour as according with probable predictions from evolution-
ary theory, the most enthusiastic among them are unlikely to believe for a moment
either that they always behave so as to maximize their inclusive fitness or that
this is what they are evolved to use their consciousness to achieve. Most humans
would assert immediately that they frequently act in ways contrary to their own
interests, even though it might be possible to show that some of the acts for which
they believed this to be true were in fact precisely according to their genetic inter-
ests, others were more or less predictable results of evolutionary novelty in their
278 { Human Social Evolution

environment, and still others were side effects of adaptive behaviour or simple
errors as a result of deficient information.
Paradoxically, we cannot say both ‘knowingly’ and ‘genetic interests’ in the
above statement, because humans in general do not know what their genetic
interests are or how to maximize them. But they do think that they know what
their interests are, just as they may think, without careful reflection, that every-
thing important about their behaviour must be conscious or readily available to
consciousness. Because consciousness is the only way of considering behaviour,
there is something that seems illogical to a conscious being about behavioural
knowledge being inaccessible to conscious consideration. This disparity is the
source of our greatest problem in understanding ourselves. It causes us to won-
der what our brains were designed to accomplish, and to suppose that there are
no challenges in everyday life that are sufficient to explain them. Jaynes (1977:
23) created an apt analogy: “It is like asking a flashlight in a dark room to search
around for something that does not have light on it. The flashlight, since there is
light in every direction it turns, would have to conclude that there is light every-
where. And so consciousness can seem to pervade all mentality when actually it
does not”.
Together with the reasons for the physical altriciality or helplessness of the
human juvenile, and our response to them (Alexander 1988, n.d.), the above dif-
ficulty may have helped cause two prominent evolutionary theorists (Hutchinson
1965; Williams 1966) to advance the notion that the intellect of humans evolved
solely or primarily to assist the juvenile in social interactions, with effects on adults
mere incidental ‘overshoots’.
The picture, then, does not fall into place in the way we would expect it to if
human consciousness had evolved as a steady improvement of personal under-
standing of one’s own behaviour in the light of the goal of inclusive fitness maxi-
mizing. We can be certain that the reason we do not yet know all about inclusive
fitness maximizing, and how the human psyche works, is not simply that the
psyche has not had time to evolve far enough in that direction. In fact, it has evi-
dently been evolving in some different direction.

CONSCIOUSNESS AND EVOLUTIONARY DETERMINATION OF

BEHAVIOUR

Consciousness is the part of the human psyche that enables us to know what we
know – or so it might seem. In actuality, it may be designed to enable us to know
certain things but not others, and to keep from us some of the things that we nev-
ertheless do ‘know’ in the more general sense of being able to act on possessed
information (see Chomsky’s 1980: 69 concept of ‘cognizing’). The psyche may be
designed specifically to keep us from knowing precisely (in the conscious sense)
what we know and what is the evolutionary significance of our existence. That
 Evolution of Human Intelligence } 279

kind of information we may have to learn from the evolutionarily novel approach
of science and technology.
If consciousness is indeed evolved, then it must be evolved to enable its bearer
to maximize inclusive fitness. If it is not evolved to bring the realisation of its
own purpose into the conscious understanding of its bearer (it is not necessary for
humans to understand Darwinian theory for some version of such understanding
to be present), then it has to be evolved to bring something different into the con-
scious understanding of its bearer. To identify this something else is surely a first
step in understanding the evolution of the human psyche.
One procedure for determining the evolutionary function of the human psyche
would be to construct a model of a psyche evolved to deliver into conscious under-
standing the direct goal of maximizing inclusive fitness and then seek to describe
the ways in which the human psyche actually deviates from this model.
Kin Recognition (i.e. measuring r in Hamilton’s, (1964) formula: k>1/r, sug-
gesting the situations in which beneficence can profitably—in terms of reproduc-
tion—be given to a relative; r refers to relatedness, k to the environmental costs
and benefits of the situation).
First, we might expect that a psyche evolved to render the human individual
acutely conscious of the goal of inclusive fitness maximizing would develop the
ability to measure the relative genetic overlap between itself and its various rela-
tives. A growing body of evidence suggests that the human psyche is indeed evolved
to accomplish this end, although not in an explicitly conscious way (i.e., the psyche
does not automatically deliver to the bearer the conscious realisation of the purpose
of the ability, or even, necessarily, the existence of the ability). In other words, any
human in a normal social situation can usually identify which of any two of its rela-
tives is more closely related to it. In part, at least, this accomplishment appears to be
carried out by some kind of counting of genealogical links. Such counting generally
works perfectly well, since each additional link halves (on average) the likelihood
of any genes possessed by one of the two relatives also being possessed by the other
as a result of their relatedness through immediate descent.
Similarly, the fact does not seem explicitly revealed to our conscious selves that
our closest relatives are either approximately or precisely 50% likely to carry any
particular gene in our own genomes as a result of relatedness through immedi-
ate descent (meaning, at least when an allele first appears in the population—
Alexander 1979: 129), and that each link reduces this percentage by one half. It is
likely that we are somehow programmed, developed, or instructed to treat relatives
as if these things were true; but we are not consciously aware of any such instruc-
tions. It is difficult to think of a way in which we could gain by being conscious
of such details (again, it is not necessary to be aware of the facts of meiosis or the
particulate nature of inheritance to approach this kind of realisation, or to possess
a ready acceptance of the significance of such facts when they do become available
to us). This realisation highlights the facts that (1) there must be a great deal of
knowledge that will do us no more good if conscious than if not; and (2) conscious
280 { Human Social Evolution

time may be restricted and valuable, so that different potentially conscious items
may compete for the available circuits. These possible kinds of limitations on con-
sciousness, however, are not the ones that most concern us here. We are primarily
interested in whether or not items or connections have been excluded from con-
sciousness specifically in the interests of preventing the conscious picture from
being complete and accurate, not simply because they are no less effective outside
conscious circuits. Said differently, we are interested in the extent to which self-
deception is a social phenomenon—a system of deceiving others through restric-
tion of self-understanding and corresponding adjustments of social signals.
Environmental Costs and Benefits (Measuring k). Continuing our description
of the hypothetical (but unreal) human psyche, designed to understand inclusive
fitness maximizing and to know about it, we might also expect such a psyche to
be evolved to develop into a superb and acutely conscious evaluator of the costs
and benefits involved in helping relatives, spouses, and friends. Again, although it
would appear that we are capable of such judgments, there is every evidence that,
when we do it, the operation is not typically brought into or kept precisely in our
consciousness. Sometimes we do indeed seem to make conscious judgements—
especially if the contemplated act is quite expensive, the returns are not anticipated
soon, or the potential recipient of substantial beneficence is a casual interactant
or a distant relative (i.e., there is considerable risk involved). Even then it does
not seem likely that all aspects of the judgement are manipulated on conscious
circuits, or that the eventual reasons for decisions are fully conscious.
Again, it could be argued that no advantage is to be gained by bringing such
details into presumably expensive conscious circuits. At some point, however, we
must begin to wonder if there are kinds of information that can be made conscious
only at a (reproductive) cost so high that selection works to exclude them even
when there may be available conscious time that is not very expensive.
On the other hand, although we have gone through the central items in
Hamilton’s (1964) formula for inclusive fitness maximizing, we seem not to have
identified any items yet for which the evolution of consciousness would be par-
ticularly advantageous or required. Nonhuman as well as human organisms maxi-
mize inclusive fitness, and neither human nor nonhuman forms appear to have
evolved a conscious realisation of the fact. So we are still equally intrigued by the
items that supposedly make consciousness an advantage in inclusive fitness maxi-
mizing and other items that would be disadvantageous if conscious.
Let us, then, consider the question from a different direction. Rather than con-
tinue trying to identify the kinds of items that we might expect to have been placed
into the consciousness of humans, let us see if we can characterize those that have
indeed been placed there, particularly in light of the manner in which inclusive
fitness is maximized and how we think about the operation of natural selection as
a result of information from the modern science of evolutionary biology.
 Evolution of Human Intelligence } 281

WITH WHAT, THEN, IS THE HUMAN PSYCHE PREOCCUPIED?

Do we use our consciousness (psyche) primarily to learn how to do the things that
incidentally maximize inclusive fitness, explicitly when other humans are the main
competitors and adversaries, and social skills are the kind we need (that is, when
other humans are the main hostile forces of nature)? Do we learn by extremely
sophisticated and complicated kinds of social-intellectual play (as practice) how to
do the calculating necessary to fulfil Hamilton’s formula, and then perhaps move
many of the actual calculations into the nonconscious, as with the actions of our
fingers in playing musical instruments (Lieberman 1984 calls this “automatization”)?
Do we also practise continually at a kind of sincere hypocrisy (Campbell 1975) (self
deception) in which we strive to present some picture other than one of seeking to
serve our own interests as individuals? If so, then how do we answer the original
question about the evolved limits of behaviour? Perhaps as follows: No human is
expected to behave in ways contrary to his own genetic interests, but all humans are
expected to believe that they do so (if asked) because, in human sociality, a continual
effort to serve one’s own interests in a conscious deliberate way is not the best way to
accomplish the purpose. It is sometimes reproductively disadvantageous (but, I stress,
not necessarily disadvantageous or undesirable in any other terms) not only to know
that one is serving one’s own interests, but even to know what those interests are.
Because social interactions are typically long-term and repetitive, because multiple
potential (alternative) partners in reciprocity are typically available, and because
motivations are often used to judge suitability of individuals for later interactions,
the most effective ways to deal with human competitors are: (1) sincerity achieved
through self- as well as other-deception; and (2) the ability to see ourselves as oth-
ers see us, so as to cause them to see us as we would like them to rather than as
they would like to. The human psyche is evidently evolved to excel at such practices.
I hypothesize that the human psyche achieves and maintains this excellence through
continual social-intellectual play—and other practice—in such forms as humour,
partying, oratory, theatre, soap operas, planning, purpose, and other kinds of social
exchanges and scenario-building. Examples are outdoing a competitor in a game or
in banter, being first in any competition that yields the prestige of being thought best
at that particular game, etc. Such play or practice involves payoffs and expenses that
are typically trivial compared to those for which successful practice can eventually
reward the player more handsomely and directly—such as the reality of getting the
job, wife, husband, friend, contract, commission, tenure, grant, award, raise, busi-
ness, farm, inheritance, etc.—thus, actually winning a disproportionate share of the
resources of reproduction and the freedom to use them in your own interests or as
you see fit. The social functions of the psyche are thus realised in (1) partial-cost play
or practice episodes; and (2) full-cost or ‘real-life’ episodes. I would venture that
recognizing the social function of the intellect, and the centrality of self-interest, is
a largely unexploited opportunity for those who would analyse human mentality in
terms of operations paralleling those of machines (i.e., via ‘artificial intelligence’);
at the least, the actual nature and complexity of the activities of the psyche seem
282 { Human Social Evolution

most likely to be revealed through analysis of social manipulations motivated by

self-interest (in the form, of course, of being ultimately genetic and reproductive).

DECEPTION AND THE BACKGROUNDS OF INFORMATION IN THE

SUBCONSCIOUS
I assume, then, that when information is pressed (or kept) out of the conscious (by
selection), this happens either because it is likely to be more useful in the subcon-
scious or because it is not useful enough to warrant saving.
Evidently, some information moves into the subconscious as a result of repeti-
tion because it no longer requires conscious effort (e.g. playing a musical instru-
ment, typing, or language). Some such information may be lost from retrieval to
the conscious (even from the memory bank entirely) as a result of disuse (e.g. a
little-used language). Still other information may never have been conscious, but
may remain in the subconscious (and be available to the conscious under particu-
lar circumstances). It may have gotten into the subconscious by a process evolved
to deal with useful information that was never conscious either (1) in the individ-
ual or (2) in the species. Or it may have been kept there by selection, in which case
the analogy by Jaynes (1977)—mentioned earlier—between consciousness and a
flashlight, would have to be modified to include that the flashlight cannot see into
every corner but does not know it.
Deception, as with any life goal, can be deliberate or conscious or not. The
conscious motive can be: (1) correct; (2) wrong because the real motive is inac-
cessible to the senses (e.g. the furthering of genic survival); or (3) wrong because
the real motive is concealed from consciousness—either it was pressed out of the
conscious or prevented from getting there.
The last must involve deception by self-deception. But why? Perhaps because
conscious intent is not needed or conscious intent would interfere. Are we, then,
ignorant of the self (genetic)-serving nature of our behaviour because (1) the true
nature of our striving is not accessible to our senses; (2) there is no value in using
the conscious; or (3) keeping our goals nonconscious aids us in serving them in
social circumstances? In each case self-deception that effects deception of oth-
ers is the aspect that I think is by far the most important in understanding the
human psyche, and the one that I will develop here. There would be no premium
on self-deception in nonsocial circumstances if this is the case, and this suggests
the beginnings of a test. The concealment of ovulation in human females is an
excellent case to analyse in terms of conflicts and confluences of interests in the
parties involved (see Alexander and Noonan (1979) and Daniels (1983)—the latter
especially for a review of published discussions following Alexander and Noonan).
Mitchell (1986) criticizes Alexander and Noonan’s discussion of deception and
self-deception in connection with concealment of ovulation as “a confusion of a
lack of information with deception”. He does not, however, seem to grasp our argu-
ment that, if an event as central to reproduction and as physiologically profound as
 Evolution of Human Intelligence } 283

ovulation—and as available to both sexes as it is in perhaps all other mammals—is

not conscious (and cannot be made conscious), there is a strong implication that it
has been kept out of the conscious by selection. Alexander and Noonan noted that
imperfect concealment—from either self or others—does not necessarily deny
that selection has favoured concealment: we simply argued that less information
about ovulation is available to the consciousness of either women or men than
would be expected if selection had not favoured its exclusion from consciousness.
If this conclusion is incorrect, then in this age of strong desires to control preg-
nancy there would surely be considerably less of a market for contraceptives.
Bernard Crespi (pers. comm.) has noted that males may react negatively to indi-
cations that their mates are aware of ovulation (implying control of fertilization
and the possibility of cuckoldry), so that human females may be evolved primarily
to avoid giving any such indication (for example, by maintaining a more or less
unchanging interest in copulation during the ovulatory cycle) rather than to be
entirely ignorant (unconsciously as well as consciously) of ovulation. This argument
actually seems to predict the precise condition that exists in modern women—
some ability to predict ovulation, but a general failure of such abilities to be acutely
conscious, or even possible, sometimes, without modern medical information.

SELF-DECEPTION, DECEPTION, AND INTERGROUP CONFLICT

Arguments that the complex cooperativeness of human social life has been driven
by intergroup competition and conflict call for all of what has just been said to be
cast in terms of intergroup interactions. I have already argued that self-deception
is a social phenomenon related to deception of others. Now I will argue further
that self-deception explicitly plays a role in fostering and maintaining group unity,
and that this role is intricated with the practice and prominence of familial, tribal,
ethnic, racial, or regional myths, including organized religion. Indeed, I speculate
that self-deception is a central factor in the group-unifying effects of patriotism,
organized religion, and similar phenomena because it leads to acceptance of dog-
mas and myths that impart, at least temporarily, unity of purpose, interests, and
striving. Myths need not represent the truth if their only significance is group
unity: they need only be accepted. Acceptance, in turn, is expected to depend not
on plausibility per se but on conviction, or acceptance, of a myth’s value in group
unification; scientific arguments about humans, for example, may be rejected
because they do not have unifying effects, yet are seen as myths (as world views,
ideologies, or even religious). Similarly, social, political, or religious leaders may
find even otherwise highly laudable goals rejected by the populace if the effect
of exhortations concerning them is divisive, restrictive, or self-deprecatory (for
example, emphasizing misuse or over-use of environmental resources or project-
ing guilt rather than pride). Acceptance of unifying myths or information or goals
depends on the individual’s acceptance of the value of group unity, including the
position or status of himself that will result, or other effects on himself and his
284 { Human Social Evolution

intimates (children, spouse, relatives, reciprocants). Even myths widely regarded

as counterfactual may be accepted, repeated, and elaborated if their effect is seen
as unifying. The extent to which directly group-unifying effects of self-deception
followed or paved the way for self-deception as a means of deceiving others within
one’s group seems moot (even self-deception with respect to one’s own likelihood
of recovering from pain or illness—in, say, a terminal illness—probably has as its
primary function deception of others).
What about self-deception in cases of maladaptively extreme risk-taking, as in
compulsive gambling or extreme heroism? In part the question seems always to be
which is (1) extreme risk-taking as a result of self-deception either (a) about the
risks directly or (b) as a result of coercion or gullible acceptance of exhortations
from others; and which is (2) inaccurate assessment of risks owing to (a) incom-
plete information (and failure to assess properly the likelihood of its incomplete-
ness), (b) inaccurate information, or (c) imperfect internal cost-benefit assessment
machinery (including developmental misinformation and pathologies such as
obsessiveness or addiction). Careful analysis of risk-taking dissected into some
such categories seems necessary to resolve this question.

EVOLUTION OF THE EMOTIONS

The emotions can be defined as various complex reactions with both psychical and
physical manifestations, as love, hate, anger, fear, grief, etc. (Webster’s Unabridged
Dictionary 1977; see also Panskepp 1982, and its following commentaries). Students
of human behaviour are apt to regard the emotions as one of the principal features
of the human psyche, along with consciousness, cognition, linguistic ability, and
personality traits.
From either logic or the above definition, one can consider the emotions as
comprising three more or less separate aspects:
1. The expression of the emotions (e.g. blushing, smiling, crying, frowning,
screaming);
2. The feelings we associate with their expression (also sometimes used in
definition, without mention of expression, as with “strong, generalized
feeling; psychical excitement” or “any specific feeling”);
3. The underlying physiological activities or changes.

Both the expressions of the emotions and the feelings associated with them
can be significant to us either when they occur in ourselves or when they
occur in others. Presumably, some of the underlying physiological activities or
changes can occur without extrinsic expression or even feelings that we might
term emotional (I emphasize the assumption that the first two aspects of the
emotions above—at least as we know and experience them—would not be
necessary for appropriate actions outside social contexts—i.e., in more or less
 Evolution of Human Intelligence } 285

completely solitary-living organisms). Also, presumably, the underlying physi-

ological activities or changes have been modified (elaborated, altered) by the
evolution of the expressions of the emotions and of the feelings we associate
with the term.
How did emotions evolve to assume their current form and degree of expres-
sion in humans?
Stage 1: It seems reasonable to assume that there was a time, in the
ancestry of humans, when the emotions were still incidental effects of
physiological events that cause appropriate behaviour in specific circum-
stances, unnoticed by other individuals; this condition probably exists
now in many or most nonsocial organisms. Such physiological activities or
changes, which prime or adjust the organism to respond in ways favourable
to its own survival or reproduction, could have (and must have) sometimes
yielded, strictly incidentally, both extrinsic effects and internal feelings in the
organism experiencing the physiological changes.
Stage 2: Incidental extrinsic changes reflecting physiological changes
must have been noticed and eventually used by other organisms. Presumably,
such observers would use the evidence of emotions in other organisms to
their own advantage rather than to the advantage of the organism showing
emotions, when there were differences in their interests. Such uses could
include fleeing if a stronger individual showed evidence of anger or likeli-
hood of attacking; taking advantage when another individual showed evi-
dence of indecision or fear; searching for evidence of danger suggested by
the emotional state of another so as to place one’s self in a more advanta-
geous position or condition, perhaps with respect to the individual showing
the emotion; etc. External evidence of changes in the emotions could also be
used by other individuals to assist them in inducing changes in the emotions
of another, presumably in directions that benefited the individual inducing
the changes.
Stage 3: Once individuals became capable of recognizing emotional states
in other individuals, then it seems virtually certain that selection would
alter both this ability and the emotional states themselves, or the external
evidence of them, in ways that would be called communicative. In other
words, as Darwin (1898) knew, at this point, the external expression of the
emotions would surely be poised to become a major source of communica-
tion, especially in social species, and most especially in species with complex
sociality in which the flow of social interactions tended to involve multiple
and rapid emotional changes among many different states. This is the point
(in evolution) at which it would become important for us to know about and
assess our own ‘feelings’ or emotions—because we could then manipulate
them to affect use by others of evidence about them.
286 { Human Social Evolution

Presumably, any organism that altered its emotional expressions under the
influence of natural selection would do so in a way that affected its own interests
positively. If the selection occurred because other organisms were already evolving
to use the incidental expressions of the emotions to their advantage, then we can
see that the organisms would tend to evolve to alter external expressions of their
own emotions in such fashions as to thwart their use by others, at least when the
others were using them to serve interests that differed from those of the individual
showing them. This means that, at least most of the time, organisms would evolve
to change their emotions in one or more of at least four ways: (a) to conceal some
emotion being experienced; (b) to suggest an emotion not felt; (c) to indicate one
emotion when actually experiencing a different one; or (d) to suggest either more
or less intensity of emotion than felt.
All of these changes imply deception or manipulation of others. But scarcely
anyone is likely to believe that all communication involves solely manipulation
and deception. One wishes to explore the question whether or not expressions
of the emotions have ever been altered during evolution in such ways as to con-
vey true feelings—to tell the truth, so to speak, about one’s emotions. Presumably,
this could happen if social partners or companions were using the expressions
of each other’s emotions to help themselves because their interests were (at least
temporarily) coincident. I presume that if two individuals sharing (at least tem-
porarily) the same interests were to detect changes in one another’s emotional
states, in each case the detecting individual would use the information in its own
interests, although such use should be imagined to include assisting either itself
(directly) or the other individual (hence, in this case, itself indirectly). Such uses
might include calming the other individual if its emotional state were placing it
(or both individuals) in danger; trying to determine what was responsible for the
emotional state of the other individual so as to respond to that environmental
factor appropriately too; making some effort directly to attain an emotional state
similar to that of the other individual if it seemed likely that the situation would
call for cooperative effort; etc. On the other hand, if the interests of two individuals
differed even slightly, we should expect each individual showing emotions to alter
their expression so as to cause the responding individual to give a slightly different
response than it might if following strictly its own interest. Situations may be rare
in which two individuals share the same interests in such ways or to such degrees
that neither can gain by deceiving the other into a little more assistance than it
would give if it were acting according to complete and truthful information about
the situation or the other individual’s motivations.
The above arguments imply that expressions of the emotions are either inci-
dental effects or else communicative, largely in the context of manipulation and
deception. They also imply that virtually any extrinsic expression of the emotions,
in an organism as complexly and continuously social as humans, is likely to have
been noticed and used enough that some evolutionary modification has occurred
in the context of communication (even non-noticeable, non-extrinsic expressions
 Evolution of Human Intelligence } 287

of the emotions are so used now, in polygraphs, or so-called lie detectors). It seems
likely that a significant effect has been caused on how we feel about what we call
our emotions. In other words, some, much, or perhaps virtually all of the ways that
we feel, consciously, when we experience what we think of as changes in our emo-
tional states, are results of emotions having evolved to be communicative. In all
likelihood, selection on the expression of the emotions has modified not only the
way we feel about our emotions, but the actual physiological events that underlie
the emotions as well. There must have been considerable feedback among these
three aspects of the emotions all during human evolution. Paradoxically, because
so much of communication, especially that involving expressions of the emotions,
may be non-conscious or even self-deceptive (as use of polygraphs suggests), it is
difficult for us to accept that physiological changes resulting in appropriate behav-
iours can occur without the feelings that we associate with expressions of the emo-
tions. This is so because the emotions have actually evolved to be communicative
and presumably would not be experienced by us in the way they are if they had not
evolved such a function. Again, the potential for confusing primary and secondary
effects is evident.
In turn, it is difficult to argue that because we blush or smile or laugh or frown
or grieve when alone (as well as when with others), this means that the emotions, as
we experience them now, are often simply ways of changing ourselves physiologi-
cally to meet nonsocial eventualities, and may not be social or communicative at
all. Presumably, however, if expressions of the emotions have evolved to be com-
municative, they may occur (secondarily) when we are alone either (1) because we
cannot easily eliminate such nonsocial expressions, owing to the insignificance
of their expense and the expense of eliminating them while retaining appropri-
ate expressions in social situations; or (2) because we have evolved to use them in
social scenario-building or planning when we are alone. It may be noticed that,
to the extent that the latter is true, expressions of the emotions when one is alone
should be honest and true reflections of at least the emotions that would be felt
in the real situation that is being modelled in a mental scenario. In other words,
truth in emotions may sometimes be expected when we are communicating with
ourselves, if in no other situation.
As noted earlier, it is significant that the communicative function of expression
of the emotions has not become entirely conscious and deliberate. Humans obvi-
ously do not have complete control of their emotions, including sexual excitement.
If the function of expression of the emotions is, as I have suggested above, commu-
nicative, then why this should be true becomes a significant question. I believe that
the answer is that, first, evidence of complete control of the emotions would indi-
cate to others that there is no reliable way of assessing the effects of social events, or
their own or others’ presence and actions, on others. Accordingly, it seems likely to
be a disadvantage in social matters to give the impression of such control over one’s
own emotions. We are in awe of actors and actresses who can produce emotions
at will, but we are suspicious and negative toward individuals who do the same
288 { Human Social Evolution

thing in our social interactions with them (consider such derogatory remarks as “I
think she is just turning on the tears!”). Anyone engaged in establishing an impor-
tant social interaction (such as seeking a long-term or lifetime mate) is bound to
respond negatively to actions making it appear that the prospective partner can
control at will its reactions to social, emotional, or sexual intimacy with us. We
expect social interactants sometimes to behave in a certain fashion despite any con-
scious intentions. We look for evidence of such effects, we try with increasing effort
to cause them to occur, and we are likely to regard their absence as evidence that the
other party is less interested in us than we would like or may require.
Accordingly, in the degree of consciousness of expression of the emotions, we
humans tread a fine line that can exemplify the aspects of consciousness that are
most difficult to understand, and that cause consciousness—which represents the
means by which we examine ourselves in the first place—be to quite poorly suited
to self-analysis, even if, paradoxically, it is the only analytical device available to
us. For it seems apparent that none of the attributes we need most to understand
if we are to comprehend our psychical nature is likely to be more completely
available to the conscious than are the emotions. The reason is evidently that
humans have evolved to be so adept at identifying falseness in deliberate (or con-
scious) actions and motivations that they have also evolved to deceive by keep-
ing many aspects of motivation out of the conscious. Even more paradoxically,
this complexity would not have arisen without the evolution of consciousness
in the first place. To use Humphrey’s (1986) analogy of the inner eye, there is no
inner eye eyeing the inner eye (of consciousness), so that we are left to analyse
these problems (create such an eye) by using the procedures of science. This is, to
some extent, a procedure advanced by Sigmund Freud. It would appear, however,
that to continue the process—to understand motivations ever more deeply so
as to understand the human psyche and all our mental activities and tendencies
more deeply as well—we will be required to refer continually to the best avail-
able understanding of natural selection, because that is the ultimate designer of
motivation.

GROUP-COORDINATION AND THE EMOTIONS

Scenarios constructed earlier in this essay for the early evolution of hominids
included three major stages (see also Alexander 1979):

1. Group-living because of predation (probably most group-living

primates and early hominids);
2. Group-living that includes cooperative group-hunting (chimpanzees,
humans);
3. Group-living that includes direct intergroup competition or aggression
(chimpanzees, humans).

Beginning with this sequence, a major question is what kinds of mecha-

nisms enabled group-cooperative humans to conduct intergroup aggression
 Evolution of Human Intelligence } 289

cooperatively. How did humans manage the coordination necessary to carry out
raids efficiently, especially against enemies belonging to their own species and
possessing the same general abilities and tendencies? What kinds of evolution-
ary change elaborated and perfected the ability to coordinate cooperative efforts
of individuals in complex fashions? Although group hunting may have been the
initial circumstance in which mechanisms of cooperation evolved, the greatest
challenges would obviously have been in connection with intergroup conflicts and
raids involving conspecifics.
Coordination of the emotions almost certainly plays a central role in group
cooperation during intergroup aggression, as it does in group hunting. Demagogues
can coordinate group emotions, and recognition of the value of leaders in such
contexts could lead to acceptance of despotism as group sizes increase. Ritual,
myth, religion, patriotism, xenophobia, ceremonies, cheerleading, and pep rallies
can all be seen as related to the coordination (and testing) of emotions in connec-
tion with specific cooperative tasks. One can hardly fail to see parallels between
the elaborate and ceremony-like expressions of excitement among diverse organ-
isms such as African wild dogs about to depart on a hunt (Lawick and Lawick-
Goodall 1971), and humans engaged in stirring their fellows to participation in
risky activities.
Robert Hinde has suggested (in a lecture at the University of Michigan, April
1987) that emotions in modern wars (as opposed to the raids of bands or tribal
groups on neighbours) are tuned not to developing and showing anger and aggres-
sive tendencies and passions but to the support of an institution (or institutions);
that patriotism, and economic, political, and religious responsibility, are called
upon by the orators and demagogues and leaders; that modern soldiers fight out
of responses to these kinds of exhortations; and that we must understand the gen-
esis of iinstitutions to understand modern war. This argument is probably slightly
over-simplified. Thus, when I was in the US Army, we were exhorted by being told,
first, that we should hate ‘gooks’ (the enemy); second, that we were, ultimately,
defending our sweethearts, sisters, wives, mothers, and children; third, that we
were, again, ultimately, defending our homes and land. (These last two exhorta-
tions were especially clear during World War II, when there were also emotional
songs about home and family, such as “This is worth fighting for!” But both were
also used when the US was fighting in Korea: “If we don’t fight them there, we’ll
be fighting them here!”); and, fourth, that we were defending democracy and all
the good institutions that are America (I also entered the Army with these final,
electrifying words from my own mother: “Although I did not raise you to be a
soldier, I know you will be a good one!’). But the idea is worth considering that—
together with the emotions per se—Hinde’s proposition can be related to the dif-
ficult problem of why despotism rises then wanes as social systems change so as to
allow or cause larger and larger groups to be unified (Alexander 1979; Betzig 1986).
Presumably, with very small groups, the emotions of the moment determine the
efficacy of a raid. Perhaps the exhortations of leaders and others, through shows
290 { Human Social Evolution

and exaggerations of their own emotions, cause everyone else to become aroused
enough to carry out a raid and do it well. Maybe increasing extremes of despotism
work similarly as group sizes enlarge—up to a point, but problems arise in man-
aging very large groups through despotism (although multiple episodes in recent
history show that in specific situations individual demagogues can be appallingly
effective). Perhaps such problems provide part of the explanation for the rise of
democracies and what I have previously called reproductive opportunity levelling
(Alexander 1987).
Surely one of the most consequential uses of linguistic ability must have been
in coordinating group efforts. And as it became significant, language would have
become a vehicle for expression of the emotions, and as well would surely have
altered their expression as a communicative device (Burling 1986).

LANGUAGE AND SCENARIO-BUILDING

Laura Betzig (pers. comm.) has reminded me of the relationship between (1) what
Hockett (1960) called “displacement” in human linguistic communication, and (2)
scenario-building as a modelling and testing activity with respect to possible later
events. Displacement refers to the human capability of communicating linguistically
about events removed in time and space from the act of communication—the use of
past and future tenses, and the discussion of events involving some different spatial
location. Although many species may have evolved some capability of building and
testing mental scenarios that involve displacement, communication between indi-
viduals about such displaced events would be exceedingly difficult without language,
and, especially, the use of past and future tenses (functionally, consideration of past
events would seem always to be in the interest of learning more about possible future
events). Displacement, so defined, is in some sense not limited to human language,
as Hockett knew: honeybee “dance language”, in which distance and direction of
sources of food or hive sites are communicated with precision and detail, is one of
the phenomena of animal communication that has most intrigued and baffled stu-
dents of human behaviour (Gould 1975). Leaving aside for the moment the problem
of comparing adequately the physiological mechanisms of honeybee and human
communication, the relationship between the rise of scenario-building in human
mental activities and the value of evolving abilities to communicate about them is
obviously worth the attention of those wishing to understand linguistic ability and
the evolution of human mentality. Lieberman (1984: 248) suggests, from the work of
Fouts, that both temporal and spatial displacement occur in the communication of
chimpanzees, through signing, with humans.
 Evolution of Human Intelligence } 291

Testing the General Hypothesis

WHAT THINGS SEEM RIGHT WITH THE HYPOTHESIS?

1. It has the potential to account for any and all sizes of socially complex
groups. Critics of hypotheses giving ‘war’ a central role in human evolu-
tion sometimes have asserted that war cannot account for the rise of nations
because different social or political groups have been at war more or less
continually without having turned their social systems into nation-states.
But this criticism misses the significance of particular kinds of expenses in
increasing group sizes in some localities—such as uncrossable mountain
ranges or rivers. An intergroup competition hypothesis includes the condi-
tion that suitable adversaries must exist to account for continual increases in
group size and complexity (see Carneiro 1970; Alexander 1979, and refer-
ences cited therein).
2. It accords with recorded history with respect to prevalence of inter-
group competition. This fact seems to me at least to shift the burden of proof
to those who would claim that prehistoric humans did not live in situations
that would have caused them to evolve tendencies and abilities to be aggres-
sive when circumstances demanded.
3. It accords with the unique human attribute of group-against-group
competition in play, and with the centrality of such play in human sociality.
I repeat my acceptance of the general theory that play represents practice
and low-cost testing.
4. It accords with the ecological dominance of the human species. This,
of course, is just a modification of the widespread anthropological descrip-
tion of humans as the species that, more than any other, creates its own envi-
ronment. As remarked earlier, I am not referring to ecological dominance of
a sort that could only postdate agriculture, but rather a kind that, except for
the presence of humans, is probably possessed even by chimpanzees.
5. It accords with the disappearance of all close human relatives despite
our rapid evolution (and probably requires it). This requirement thus
approaches becoming a falsifying proposition (that fails: see also, comments
below on apes and dolphins).
6. It accords with the ‘autocatalytic’ model of brain size increase (Stringer
1984). Of course, internal changes in the brain that increased intellectual
capacity were surely occurring simultaneously with increases in size of the
brain itself, or of the brain cavity; and, as already noted, it is possible for
social structures to be achieved in which strong selection for increases in
brain size might taper off and disappear, as the fossil record suggests.
292 { Human Social Evolution

WHAT THINGS SEEM WRONG WITH THE HYPOTHESIS?

1. Early humans and pre-humans are generally assumed to have very

low population densities—too low for intergroup competition to have been
significant (e.g. Martin 1981). We must, however, wonder how much of
this assumption is due to inadequate information, and to the tendency to
assume a priori that weather, climate, and food were early humans’ greatest
problems. To maintain my argument I have to conclude that densities per se
were not critical, or else that estimates of densities were wrong. It is probably
more important to know what kinds of social groups people lived in, and
why, than to know densities per se. We must consider the possibility, I think,
that social groups may have been in intense competition with one another
for scarce or localized resources even if overall population density was
low (e.g. Ember 1978). Hamilton (1975) has stressed that life in small kin
groups—such as presumably would occur under low population densities—
could well exacerbate the tendency to be ethnocentric and xenophobic.
The question of densities also seems to bear on hypotheses about rates of move-
ment between geographic regions, and thus would appear to bear on the alterna-
tives of (1) a multi-regional hypothesis involving a single species in which genetic
(or cultural) changes appearing in a few or many separate localities are repeat-
edly spread throughout the species; or (2) a single-locality hypothesis involving
appearance of either a separate species or a strikingly different form in one local-
ity, spreading without much (or any) interbreeding to cover eventually the entire
range of modern humans and replacing the forms previously living there (e.g.
Wolpoff, this volume). Either of these alternative hypotheses is compatible with
the hypothesis advanced here. Intergroup competition could have been (and prob-
ably was) between both conspecific social groups and similar species.
That humans reached Australia and New Guinea about 40 000 years ago—
apparently across a sizeable stretch of water—and penetrated to southern South
America after crossing the Bering Strait 10 000 or 15 000 years later, and also the
broad overall distribution of evolving hominids for several million years, implies
considerable ability of hominids to move great distances—hence, to interbreed,
and to interact with strange groups. It also implies a strong likelihood of evolution
according to the amity-enmity polarity of intergroup competition as outlined here,
regardless of actual densities or general way of life. Only a close intragroup coop-
erativeness, leading almost automatically to intergroup hostility, is necessary. The
entire recorded history of humanity, and our direct knowledge of ethnocentricity
and xenophobia (see Reynolds et al. 1987), is also consistent with these implica-
tions, hence, in this sense, with the general hypothesis developed here.
2. Early humans and pre-humans are generally assumed to have been
under great food stress. There is, however, more than one reason for food
stress. As others have pointed out, a dominant male in a highly polygynous
 Evolution of Human Intelligence } 293

species, at the height of his breeding performance, is almost certain to be

under ‘food stress’. So may be a subordinant male, ostracized from his social
group by a dominant male or for any other reason, or a subordinate group.
3. War and large groups are both recent; as discussed below, however,
there is no unambiguous evidence of either early aggression or its absence.
4. Great apes have some of our mental attributes, including a kind of
self-awareness (Suarez and Gallup 1981), but perhaps only chimpanzees cur-
rently have an appropriate social structure. It might be possible to argue that
orangutans and gorillas do not have intellects that are sufficiently like those
of humans to require (by my hypothesis) that they have lived in social groups
that would have caused the kind of runaway intellectual evolution I have
been describing. But I cannot easily reject the notion that the intellects of the
great apes may in fact demand explanation in terms of my hypothesis. I am
led, then, to wonder—entirely without empirical evidence—whether or not
orangutans and gorillas once lived in social groups more like those of chim-
panzees and humans than is presently the case: in other words, multi-male
groups, and perhaps multi-male groups in which the males were coopera-
tive in hunting, or even in intergroup aggression (see Wilson 1975: 568, and
Wrangham 1987: 60, for comparisons of some relevant attributes). Wilson
(1975: 36) suggests that orangutans may have once been more social than
they are now, and that conditions leading to extreme sexual dimorphism
(exaggerated in both orangutans and gorillas) may have reduced sociality
(Ciochon 1987) summarizes information on ape and hominid phylogeny,
and Robert Smuts has suggested to me that juvenile orangutans may be more
social than expected from the current social life of the species.
5. The problem of explaining the size and complexity of dolphin brains,
and their apparently remarkable learning abilities, parallels that of under-
standing the great apes (Connor and Norris 1982; Schusterman et al. 1986;
Herman 1980; Connor, pers. comm.). Dolphins may be as unusual in these
respects compared to other inhabitants of the sea as humans (or humans
and apes) are compared to other inhabitants of terrestrial habitats (e.g.
Worthy and Hickie 1986). Dolphins do not construct tools or other com-
plex artifacts. They are evidently subject to severe predation from sharks
(Krushinskaya 1987), and are remarkable navigators (Kellogg 1958; Norris
et al. 1961; Klinowska 1986). If these features of their environment are not
responsible for their large brains and apparently complex mental abilities
we are left with the complexity of their social life by default. Unfortunately,
because of rudimentary knowledge of the details of everyday dolphin soci-
ality (Norris and Dohl 1980; Krushinskaya 1986), we can make little fur-
ther comment on this topic. This ignorance, coupled with the unusual brain
and learning abilities of dolphins, has caused a great deal of public inter-
est and considerable speculation among scientists (for example, the highly
publicized speculations about dolphin communication, and hypotheses
294 { Human Social Evolution

that dolphins may engage in reciprocity (Connor and Norris 1982) and that
odontocetes may stun their prey with high-intensity sounds (Norris and
Mohl 1983; Morris 1986)). The importance of examining both dolphin and
ape sociality more intensively seems apparent.

HOW CAN THE HYPOTHESIS BE FALSIFIED (BEYOND THE ABOVE

DIFFICULTIES)?

1. One obvious possibility of falsifying the general argument that humans

have evolved largely through a process of runaway social competition and
imbalances of power between competing groups would be to show that such
activities are too recent in human history to account for evolution of humans
from nonhumans or for evolution of modern humans from archaic humans.
I think that most accounts of human social evolution (e.g. see Mann 1986,
and references cited therein) imply that this is in fact the case. If, however,
chimpanzees have already embarked upon a path involving significant inter-
group aggression—a proposition developed independently of the argument
generated here and earlier (compare Alexander 1967–1988, with King 1976;
Goodall 1986; Wrangham 1987; and Manson and Wrangham, n.d.), then
this potential falsifier, it seems to me, is itself falsified. Nevertheless, it seems
necessary to understand how it might be that current accounts of the evolu-
tion of civilization do not always seem to support the ideas I am espousing.
Part of the reason may result from views about hunter-gatherers that may be
untenable (e.g. see Ember 1978; Alexander 1979). A second part involves the
nature of evidence about intergroup aggression.
2. Absence of indicators of significant intergroup aggression is a second
possible falsifier of my arguments. My previous comments on this question
(Alexander 1979: 227–228) are here paraphrased and supplemented:
Two kinds of evidence bear on the question whether or not intergroup compe-
tition and aggression have played a central role in human evolution. One kind is
physical evidence of aggression, including fossils. Little or none of this evidence is
unequivocal: spear points, arrowheads, and stone axes all have been called ‘tools’
or ‘weapons’, depending on one’s bias, and they could have been either or both;
skulls could have been crushed by predators or damaged after death; evidence
of cannibalism could have been interpreted differently if it came from ceremo-
nial affairs within groups rather than from wars; etc. For example, as suggested
by Darwin (1871), Pilbeam (1966), Wolpoff (1971), Lovejoy (1981), and others, in
the light of the evidence that humans are willing and adept at complex inter- and
intragroup competition, stone ‘tools’ (weapons) could have lowered the usefulness
of teeth as weapons (of defence or offence, and against predators as well as conspe-
cifics) as much as (or rather than) “removed the need for use of the anterior teeth
 Evolution of Human Intelligence } 295

in aiding the hands to hold various utensils or materials such as skin or wood”
(Howells 1976).
Even continuous intergroup hostility and aggression do not necessarily leave a
record for archaeologists to trace. If there were no written records, what evidence
would there be to tell us what happened to the Tasmanians and the Tierra del
Fuegians? Without written records could we have been unequivocal thousands
of years later about what the invading Europeans did to the Native Americans on
both continents of the New World? Consider the most monstrous cases of geno-
cide in recorded history: can we even be sure, again without written words, that
what happened in the twentieth century at Buchenwald and Auschwitz, and in
Nigeria and Cambodia, would be properly interpreted, say, a million years from
now? Yet more people may have been killed in these places than existed in all of
the time before recorded history. Such questions, it seems to me, cast doubt on the
interpretation that equivocal evidence of human aggression, not to say the milder
yet potentially continual and crucial forms of intergroup competition, must auto-
matically be discarded.
The second kind of evidence comes from interpreting recent history and the
behaviour of modern humans, and then asking about the legitimacy of extrapo-
lating backward in time, both to postulate what happened and to interpret the
otherwise equivocal evidence from archaeology and palaeontology. We know
that intergroup competition and aggression have been continuous across nearly
the whole face of the earth throughout recorded history. We know that coop-
erativeness on the grandest scale, and the greatest of all the alliances of history,
were in response to upsets in balances of power and the aggression of one nation
against another. We know that competition is continuous among the various kinds
of political groups, large and small, that exist across the whole earth. We know
that atomic fission, space travel, and probably most of the remarkable modern
advances in science and technology occurred or were accelerated as a consequence
of intergroup competition or outright war.
Not only are there two kinds of evidence with respect to intergroup aggression,
but the nature or effects of intergroup aggression on human evolution may be
better understood if it is considered in at least two major stages. The stage that is
more understandable to us, and better represented by evidence, is the later stage,
involving organized military interactions, extensive weaponry and strategizing,
armies, and sometimes very large scale operations. This is the kind of intergroup
aggression that is typically called ‘war’. It extends from the beginnings of recorded
history to the present, virtually continuously, is often highly organized and com-
plex, and was evidently instrumental in the development and maintenance of the
kinds of social systems that have prevailed across recorded history. As already
mentioned, these facts place a certain burden of proof on those who would have
intergroup aggression disappear as one moves back into prehistory.
Intergroup aggression prior to recorded history is more difficult to substantiate
directly. As already suggested, tools may have been weapons, and most evidence is
296 { Human Social Evolution

equivocal. It seems legitimate to consider chimpanzees as approximating a model

of some early stage of such aggression. The time between such a stage and the
appearance of full-fledged ‘war’ could have involved several hundred thousands of
generations and, at times, more than a single species. It would have been during
this period that the transition from the pre-human to the human condition would
have occurred.
3. Show that, historically, the topics, timing, or sequences of representa-
tional ability (evidenced by tools, weapons, art, ceremony) are wrong; or,
by other means, that the complexity of the psyche is not tied primarily to
success in social matters.
Any interpretation of the function or operations of the modern human psyche,
and of its manner of evolution, must be compatible with the fragments of evi-
dence that exist in fossil or other forms (tools, sculptures, paintings, evidence of
planning and social structure, items associated with burials, and what is known
about the behaviour of nonhuman primates). Meanings appropriate to the rest of
the arguments must eventually be derivable from the nature of the artifacts, their
ages, and their sequence. One wishes to ask whether or not evidence of appropri-
ate representational ability appears at the right times and in the right sequences
during human history to support the arguments here generated. What are the (1)
real and (2) expected sequences of changes in the fossil and other evidence of
scenario-building (as well as tool- and weapon-use and social structure) across
the relevant periods of human evolution? When and how did scenario-building
ability become a means of acquiring status—as in sexual selection or leadership?
What kinds of findings would support or falsify the ideas expressed here? Two
kinds of evidence are available to us on this question: (1) indications of changes in
sizes, compositions, and interactions of human social groupings leading toward
the ranges of variation found in modern humans; and (2) artifacts, fossils, and
remains relevant to psychical abilities of the sort found in modern humans. How
can they be used to test the arguments advanced here? The seminal contributions
to this projected test appear to be those of Wynn (1979, 1981) and Gowlett (1984).
Using the artifactual record, these authors begin tracing the gradual appearance of
consciousness, self-awareness, foresight, and the internal representational abilities
of modern humans. Although the data are sparse, they are at least able to suggest
that Homo erectus, as we would also imagine from its phylogenetic position, pos-
sessed an elaborated kind of ‘great apes’ mentality appropriate to the predecessor
of modern humans. So far as I can tell, the meagre evidence from this kind of
analysis as yet casts no doubt on the hypotheses advanced here.
4. Show that the greatest increases in intellectual or mental capacities
(brain size?) occurred when nonhuman or nonbiotic hostile forces
were most severe rather than vice versa. To me this test seems the most
unequivocal, and the most likely to be useful (see Stringer 1984). It
requires evidence as to whether or not the greatest changes in intellect
 Evolution of Human Intelligence } 297

occurred during maximum extent of glaciation (and near the glaciers

or in otherwise severe—perhaps xeric—climates), and when population
densities were lowest as a result of such extrinsic hostile forces; or on
the other hand under mild climatic conditions when food was relatively
abundant and population densities were highest.

Additional tests may be possible from psychological studies that bear on the
use of the human intellect in social matters versus other circumstances. No such
test is obvious to me now, since it would appear that usefulness of the brain in
other circumstances may have evolved concomitantly in such fashion as to render
inextricable the two aspects of brain function. I suspect, however, that continued
confirmation of the significance of the emotions and personality traits in social
and communicative matters, and especially in manipulating and deceiving oth-
ers, would provide strong support for the arguments advanced here. This will be
especially true if such features of the psyche are also related to linguistic ability
and the various aspects of consciousness and cognition in ways that reinforce the
argument for social significance.
When I described to a friend the problem of titling this essay about the human
psyche, he suggested with a sly smile that I might call it “Psychology”. Having
completed the essay, I discover that, indeed, I have argued, in agreement with
Humphrey (1976–1986) and using his phrase, that the function of the human
psyche is to “do psychology”—that is, to study itself as a phenomenon, in ourselves
and other conspecific individuals, and to manipulate, in particular, the versions
of itself found in those other individuals. When I read this statement back to the
same friend, he nodded and added, “Unconsciously”.

Acknowledgements

I thank Theodore H. Hubbell, Richard C. Connor, Robert W. Smuts, Donald

Symons, Pat Overby, Lars Rodseth, Laura Betzig, Martin Daly, Margo Wilson,
George C. Williams, William D. Hamilton, Daniel Otte, Robert Foley, Katharine
M. Noonan, Mark V. Flinn, Paul Turke, Cynthia K. Sherman, Paul W. Sherman,
John Speth, Bernie Crespi, Kyle Summers, Randolph M. Nesse, Milford Wolpoff,
and Frank Livingstone for stimulating discussions on this and related topics, and
for help with the manuscript. Joseph Manson and Richard Wrangham allowed me
to discuss their unpublished manuscript. Bernie Crespi and Aina Bernier helped
immensely with the literature search. Richard C. Connor, in particular, assisted in
developing ideas about reciprocity and the stratification of coalitions. Financial
support is acknowledged from the Frank Ammerman Fund of the Insect Division
of the University of Michigan Museum of Zoology, and the Evolution and Human
Behavior Program of The University of Michigan College of Literature, Science,
and the Arts.
298 { Human Social Evolution

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11

Evolution and Morality

Injustice

and the continuing weight of conscience

I, for one, cannot deny having used,
if only long ago, and senselessly cued,
places of origin, shapes of eyes, colors of skin,
to set myself apart from other men
those whose greatest breaches with me
were fashioned through a history
of bullying and slavery and penury
that in some cruder, crueler times
were started by those self-same signs.
Alexander 2011, p. 25
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 INTRODUCTION

Twelve (More) Things about the Evolution of Morality Make

People Nauseous
David C. Lahti

“Over there they believe society is based on lies, but here we believe in justice.”
That is essentially what I was told by an experienced graduate student at the
University of Michigan when I mentioned that I was going to visit Dick Alexander.
When I arrived in the orthopteran range at the Museum of Zoology, eight or nine
backs were hunched over a new Nature paper looking for a fatal error (Keller &
Ross 1998). It seems that a “green beard”—a previously hypothetical trait that is
claimed to indicate relatedness accurately and that individuals can recognize in
each other and use as a signal for preferential treatment—had been discovered in
the red fire ant Solenopsis invicta. Perhaps the experimental odor transfer control
hadn’t been done perfectly. Perhaps they used the term “outlaw gene” (Alexander
& Borgia 1978) too loosely. But all the elements were there! Queen ants that
reproduce have a genotype Bb. Queens with a BB genotype attempting to repro-
duce get killed, primarily by those with the Bb genotype, who can tell the alleles
apart via cuticular hydrocarbons. Fine, it’s probably a real green beard in nature.
But theorists have warned that such a system is vulnerable to cheating. A BB ant
might eventually masquerade with the Bb signal, if it is possible to separate those
two effects of the gene. Deceit would be adaptive for BB ants. Later I hesitantly
raised the objection that any deceit, or even concealment for that matter, might be
hard to maintain long term in the face of others’ interests in uncovering the truth.
“Does your wife know when she is ovulating?” retorted one graduate student.
No, I admitted. Of course she can learn to do so, but only because of modern
medical and physiological advancements that have revealed the very existence of
ovulation. And yet how important ovulation is to reproduction! And how flam-
boyantly some other female apes advertise it! So why do we conceal it? Very inter-
esting. Then I read the so-called Uniquely unique paper (Alexander 1990), which
had been published as an unprecedented Special Publication of the Museum of
Zoology because it was deemed too controversial for the ordinary Occasional
Publications (You have got to be kidding me, I thought—but I suppose I’d rather a
paper of mine be considered Special rather than merely Occasional). I was shortly
convinced that hiding the truth, not only from mates but even from oneself, was
adaptive for female humans in the case of ovulation, as it made males more likely
to pair-bond and provide biparental care, features so important in our socially
308 { Human Social Evolution

competitive environment. Adaptive deceit in ants, adaptive evasion in humans:

We’re already getting close to a society built on lies and I’ve only been here one day.
No wonder the ecologists for social welfare across the street warned me. But it’s too
late now.
Why do we see resistance to understanding ourselves evolutionarily, even
among those (like those ecologists) who broadly understand and accept evolu-
tion? Alexander, whose synthetic evolutionary approach to human culture is
the most extensive, careful, and consistent around, has returned to this question
repeatedly, especially in recent years (Alexander 1978; Alexander 1988; Alexander
2005; Alexander 2009). I’d like to focus this question further here and apply it spe-
cifically to our understanding of the origins of morality, especially the understand-
ing that has been promoted by Alexander’s own work. The paper “Biology and the
Moral Paradoxes” (this volume, and Alexander 1982) is a succinct and effective
summary of the aspects of Alexander’s thought that can lead us into the resulting
controversy and resistance.
One fascinating and frustrating phenomenon is that those who study morality
professionally are among the least likely to understand or accept our best the-
ory of the evolution of morality. I would argue that this rejection is not primar-
ily because of anything they know about morality that evolutionary biologists do
not (although that is certainly the case, and a problem that should be redressed).
A more pervasive and general reason is simply that most philosophers and social
scientists still practice their arts as though humans are not a product of evolu-
tion. This is astonishing and becomes more so with each passing decade. However,
aside from their attitude that evolution in general is irrelevant, their specific loath-
ing and dismissal of the emerging picture of the evolution of morality needs spe-
cial explanation; and I argue that this attitude is not at all surprising and is likely
to continue for a long time. Even many biologists who do not think much about
human evolution have a similarly negative response to evolutionary moral theory,
almost by default. I think the main reason for the nausea is that our best theory
of the evolution of morality looks as though it were concocted precisely for the
purpose of slapping moralists in the face, making fun of goodness, and dragging
through the mud everything pure and decent in the world.
Before we get to this, however, there are several arguments the professional
morality folks use to stop evolutionary analysis before it even starts. Most of these
have already been discussed to death and I will not deal with them again here: a
group of doubts about the explanatory efficacy of science in general or evolution-
ary science in particular, including concerns about the nature of history, social and
other influences that compromise objectivity, and the cute postmodern idea that
science might simply be one of many possible narratives; another family of con-
cerns encompasses metaphysical or religious (including political and social theo-
retical) taboos about “human nature,” including a preference for absolute freedom
of the will, worries about genetic determinism, throwback Marxist hopes, or just
a general distaste for inherited influences on the human mind. These venerable
 Evolution and Morality } 309

arguments could be parsed into a dozen perceived problems with an evolution-

ary approach to morality. I will leave those aside here in favor of another dozen.
Actually, the first two remain in this general show-stopper category, often surfac-
ing as peremptory blurts. I will consider them only briefly: That evolution may
well happen but it is irrelevant to philosophy, and that a lack of consensus is an
excuse not to think about the issue.
Philosophers frequently sniff at (1) the outrageous suggestion that evolu-
tionary biology has anything at all to say about morality. Such a radical sepa-
ration of science and philosophy would have been alien to nearly all the great
philosophers of old, including Aristotle, Descartes, Hume, and Kant, who were
inspired by the latest empirical knowledge and stretched its implications as far as
they could into a springboard from which to leap into realms that science had not
yet fathomed. A few philosophers still retain this idea of science as handmaiden
to philosophy. How different Wittgenstein, who was so content with a narrow
conception of philosophy that he could write (and I am so sick of seeing this
quoted) that “Darwin’s theory has no more to do with philosophy than any other
hypothesis in natural science” (Wittgenstein 1921). I respect Wittgenstein’s exper-
iment in philosophical minimalism, in the spirit of the beginning of Descartes’
A Discourse on Method (1637). But should philosophy really be nothing but con-
ceptual clarification? No. Philosophy, ILORVRILD, is literally the love of wisdom,
it is the search for answers to the big questions. And it has a responsibility to take
all human observation into account in order to do this. Your concepts them-
selves, philosophers, depend on your psychology, that is to say your minds, which
are a product of history and have evolved genetically and culturally according to
particular rules for particular reasons in particular environments. Your concepts
would be different if any of those things were different. To practice philosophy
as if conceptual clarification can be done in ignorance of human natural history
is to assume an idiosyncratic human natural history of your own, one that prob-
ably dates back to Hume or even to Plato, and represents the best of what they
knew about humans. To engage in metaphysics without understanding human
evolution is to assume a false preevolutionary anthropology. To engage in moral
philosophy without understanding human evolution is to assume a false preevo-
lutionary psychology and sociology.
Alexander, building on the progress of other evolutionary biologists such as
Darwin, Williams, Hamilton, and Trivers, has birthed an expansive and vibrant
philosophy, representing the first several steps in a reevaluation and recasting
of the world’s big questions in the light of evolution, including those relating to
morality (e.g., Alexander 1979; 1982; 1987; 1989). Of course Alexander, like many
scientists, considers it a slight for his work to be referred to as philosophy, which
everybody knows is a code word for a pompous and meticulous web of utter
speculation. This is not philosophy at its best, however. Philosophy is an art of
precise and internally consistent hypothesis generation. And the more there is to
be explained, the more good philosophizing is necessary in order to develop a
310 { Human Social Evolution

hypothesis that is broad and detailed enough to explain it. Philosophizing about
something as formidable as human nature must amount to the generation of a
large ball of interacting hypotheses, all of which are consistent with each other and
explain all observations to date.
Another case rather shamelessly proffered by professional thinkers about moral-
ity is that (2) the difference of opinion among evolutionary biologists as to the
explanatory power of their field with respect to morality gives the rest of the world
an excuse to let the matter sit. Certainly there are many theories out there, and
everyone has a twist: cognitive scientists, psychologists, a diverse array of anthro-
pologists, primatologists, economists, journalists, and yes zoologists. Some treat-
ments are better than others, most are rhetorically overblown and oversimplified,
and (to be frank) few of them deserve to have seen the light of day (Lahti 2003). If
the students of evolution can’t even get it straight among themselves, why should
philosophers and social scientists be concerned? Of course, this logic is especially
dangerous for philosophers to use because there is not a single important matter
in the world on which there is a reasonable consensus among their own ranks. The
fact is, although science does proceed socially by consensus, no philosopher nor
scientist can get any sort of answer to any big question by depending on, much less
waiting for, consensus. The bigger the question, the more difficult wrapping one’s
head around it becomes, the more axes are out there to grind, the more diverse is
the field of ideas, and so the poorer the consensus. Humans will always fret and
explore most intensely about issues that have to do with humans—that’s almost a
truism. Rather than letting the matter sit, we must compare the extant hypotheses,
winnowing them for consistency, explanatory power, and their ability to pass tests
having the potential to falsify them.
Provided that evolutionary analysis of morality is actually allowed to begin, any
serious work might very well meet with a turned-up nose regardless of what the
final picture looks like, because of a three-pronged arsenal of arguments, almost
like an immune defense. First we have the lingering effects of a prior infection: (3)
guilt by association with “social Darwinism.” In the early days, some theorists
attempted to derive morals from the evolutionary process, some of which claimed
some humans to be better than others and justified power disparities and social
injustices. Such detestable ideas had the effect of virtually inoculating the acad-
emy against susceptibility to any future outbreaks of evolutionary thinking about
morality. Even today, the mere mention of the term “social Darwinism” exerts
great rhetorical power, whether it is used appropriately or not. If for some reason
that prophylactic doesn’t do the trick, the second line of defense against evolution-
ary ethics is to take two fallacies and call a philosopher in the morning. The two
fallacies in question do highlight actual errors of thought when used properly, but
with regard to the connection between evolution and morality they can be por-
trayed as having mighty accusatory powers far beyond their logical reach. One is
(4) the genetic fallacy, where the origin of an idea is used as an argument about
its validity or truth. All you have to do (some think) is accuse someone of this, and
 Evolution and Morality } 311

they will be prevented from considering the origin of morality to have any rel-
evance for . . . morality. Wielding (5) the naturalistic fallacy can be just as vital. This
fallacy is committed whenever (depending on its formulation) someone claims
that moral values are implied by, are defined as, are really the same thing as, or
somehow arise out of, facts of the sort that natural science can countenance. Some
take this fallacy to absolutely debilitate any attempt to make morality natural, or
rooted in things that are accessible to natural science, which presumably includes
anything that has evolved. With this arsenal in place, the professional students of
morality might not have needed much else in order to protect their subject from
evolution. (Someone should name a fallacy for the reckless wielding of fallacies.)
However, strange as it may seem, these defenses against evolutionary biology’s
intrusion were probably not even necessary: Evolutionary biology became its own
worst possible publicist.
To start with, although evolutionary biology does not preach a morality, it
describes the human condition in the context of that of all life, where traits persist
and spread insofar as they benefit their individual bearers. Thus, any consistent
explanation of human action from evolutionary biology will look like (6) egoism,
which is often considered “knockabout philosophy” as my philosophy advisor
used to use the term—a view you toss around to whet the critical abilities of young
thinkers, but eventually discard for more serious contenders. Still, there are always
plenty of “enlightened” egoists around, people who believe that in some way what
is good is so because (or consists in the fact that) it is good for us. The horrifying
part is the particular meaning of “good for us” that evolution brings to the table.
This is where evolutionary biology irreparably ruins its image. What we humans
consider good, we came to consider such because . . . it is good for . . . (7) reproduc-
tive success. This means, for starters, sex. After thousands of years of morality being
a vanguard against . . . well, immorality if you know what I mean, we are asked to
believe that the two have always been in bed with each other! The idea that moral
goodness or rightness has any sort of basis at all in making babies—no, worse, in
making more babies than other people do—is probably the most odious thing any
thinker could suggest about the nature of morality. Or, if there were a more repul-
sive connection, it would have to be the other thing we protect our children from
in the name of goodness: (8) violence, and especially war. And lo and behold, this
becomes in the evolutionary picture the sine qua non of morality! All of nature
struggles to reproduce, but only humans have morality. Why? Because we humans
have lived in social groups that have competed so fiercely with each other that it led
to arms races, not only of literal weapons but also, and more crucially, of minds. We
outsmarted other hostile forces to become each other’s worst natural enemy. And
the group competition was so unrelenting that the social group had to be unified
or else disintegrate. Any individual’s successful reproduction would depend on the
persistence of the group, necessitating cooperation with other group members, and
standards for such cooperation, including to some extent the sacrifice of immediate
individual interests for the greater good. Thus, paradoxically, war led to goodness,
312 { Human Social Evolution

and without war we would never have evolved the intellectual ability to decry war,
nor to hope for something better. Moreover, the mechanism by which this hap-
pened was a “selfish” maximization of individual reproductive success.
What should be our response to repugnance at this history? In my opinion, our
response should be to encourage quality science education so that the repugnance
declines with time. As morally ambiguous as this proposed history is, it is our
most powerful explanatory framework for human nature. Those who understand
natural selection and appreciate its implications, and who are aware of the nature
of social behavior in other species, are not likely to encounter a tremendous barrier
to realizing or accepting this picture. And at this point, despite evolution-inspired
nihilistic popularizations, those who respect morality and the idea of goodness
might still rescue them in dignity from the rubble of their history. After all, egoism
in an evolutionary sense includes concern for one’s kin and group, reproductive
success for humans includes not only sex but pair-bonding and parental care, and
fighting only sowed the seeds for morality insofar as it protected one’s social group
and became the wellspring of cooperation. More generally, many human traits
derive from precursors that were humbler in some (anthropocentric) sense. Just
as many of us have risen above a Wilberforcian indignance at the idea of having
evolved from animals that don’t wear clothes or speak very well, maybe we can
stave off moral discomfort at the centrality of selfishness, sex, and violence in our
moral evolution.

This is not the end of the story, however. The foregoing is prudish stuff com-
pared to the next level at which moral ambiguity enters the evolutionary picture,
the full extent of which many philosophers and social scientists are not even
aware, so poor is the diffusion of ideas across disciplinary borders. This is the level
of the individual human psyche, and of the motivations or intentions that guide
our actions. For morality to have fulfilled its ancient and continuing evolutionary
function (thus explaining its persistence in the repertoire of the human species)
we can expect (9) a correlation between the interests of the genes and the goals
driving human action. To the extent that reproductive success has been the cur-
rency of natural selection, it will accordingly have evolved to be a predominant
and universal human aim. And to the extent that group competition has been the
engine of cooperation, corresponding desires and motivations will have evolved
in our psyche as well. Moreover, any exceptions or supplements to this picture
are not expected to be universal or particularly lasting. Views and people going
against this trend will be statistical residuals in the long view. What this means
for human psychology and personality is morally complex: We are expected to act
primarily to benefit ourselves individually, as well as our mates and offspring, and
(because of indirect fitness benefits) our nondescendant kin. We will tend to value
members of our own various social groups over nonmembers, and we will tend to
withhold beneficence and be less caring the more distantly related people are to
us. Some of these tendencies and the implications from them we might consider
 Evolution and Morality } 313

morally praiseworthy, others acceptable, and many we would consider immoral.

There is no consistent explanation for the evolution of moral behavior—rather,
there is the explanation for the evolution of human behavior, including the moral
and immoral mixed up together.
To such standard material from the Alexandrine picture of human behavior we
must add still more troubling consequences from the interaction between group
competition and indirect reciprocity. Indirect reciprocity, the mechanism by
which rewards and punishments can return to someone through any individual in
society or even from society as a whole, is the most pervasive and explanatory ele-
ment in the evolutionary analysis of morality (see Sigmund, this volume). While
still yielding falsifiable predictions, indirect reciprocity renders unproblematic a
majority of the scenarios that are typically offered to challenge to the evolution-
ary picture, from blood donation and philanthropy to monasticism and celibacy.
Considering the benefit of group unity, indirect reciprocity becomes a vehicle for
widespread social pressure to contribute service to the group. Not surprisingly,
much of what we consider moral or good tends to be consistent with this rubric
of service to the group. Insofar as group cohesion preserves the group, it benefits
the reproductive success of its members; consequently these members will tend to
benefit by serving the group, encouraging this group service in others, and socially
enforcing their commitment. However, more broadly, each individual will also
gain in reproductive success within the group by seeking benefits for oneself at the
expense of others in the group. The result of this analysis is that each individual
should encourage in others a greater level of commitment to group service than
one’s own optimal level of commitment. Moreover, by the mechanism of indirect
reciprocity it is less the actual good behavior or intentions that lead to reproduc-
tive success, and more the perception by others that one is good. Thus we are likely
adapted to inflate the impression we lend to others of our goodness. The evolu-
tionary prediction in short is that (10) hypocrisy is inherent in human nature
and an essential part of adaptive moralizing. Many adaptive strategies can be
drawn from this prediction, including ways to discriminate in our dispensing of
benefits, to play upon the altruism of others, and to anticipate and manipulate
others’ impressions of us for our own gain. The discussion of morality has turned
into a discussion of how we get around morality, and the evolution of goodness
has turned into the evolution of the best tool in the con man’s kit. Thoroughgoing
goodness doesn’t exist except in the sucker, and so those of us in the know have
every reason to exchange evil grins and high fives (or perhaps more prudently,
discreet winks) when we encounter idealistic people who really appear to have
some respect for the concept.
Actually this is not quite right. According to the emerging evolutionary pic-
ture of morality, the main reason we do not see so many evil grins and high fives,
or even winks, in response to others’ moralizing or greater group service than
our own, is more than just prudence. It is possible that some or even most of
us do not generally stifle obvious feelings. Alexander’s more likely alternative is
314 { Human Social Evolution

(11) self-deception. We are not perfect at hiding our conscious motives, and others
are evolved to detect them. Therefore the mechanisms just described work better
when we are just as clueless as our audience is, to the reasons why we have come
to encourage moral adherence and laud heroism. (Hence, Alexander adds, our
resistance to accepting those mechanisms [Alexander 1987].) We tend to be con-
scious of things when being conscious of them is advantageous, and not otherwise.
(Note that modern psychology has it backward when it concentrates on why we
sublimate or render certain events or motives unconscious, when this is in fact the
primitive and much more widespread state of affairs in nature. The real question
is why our ancestors became conscious of certain things.) This incomplete and
even false knowledge about ourselves allows most of us to have the comfortable
sensation that we are unitary and consistent in the causes of our actions. Many
lines of research have since converged on this idea that we humans are inher-
ently inconsistent and either cognitively fragmented or self-deceived. The idea has
an array of explanations in the literature besides the facilitation of moralizing: is
it also because we have old and young parts of our brains, or two lateral halves
(Haidt 2006)? Or is it because we have some genes inherited from dad and some
from mom and these can predispose us differently (Burt & Trivers 2006)? Or is
it because our brain is comprised of modular neural networks that evolved for
different and often contradictory functions (Kurzban 2010)? Whatever factors
besides selection for moral manipulation contribute to our “impurity of heart”
(Kierkegaard 1846), the upshot for our psyche is that we are far from the internally
consistent and honest wills that we generally consider ourselves to be. Worse, in
a sense our hypocrisy probably runs even deeper than a temptation or felt prefer-
ence—it may run so deep that it is cognitively inaccessible to us, while its guidance
of our action is nevertheless successfully operating in our day to day lives.
With this, even many who respect the role of evolution in human psychol-
ogy and behavior have had enough. The paradox that egoism lies at the base of
altruism, that self-regard somehow subsumes other-regard, is morally ambiguous
enough at the level of evolutionary mechanism. For it to threaten much more seri-
ously to undermine our integrity at the level of individual thought and action is
just too much. Altruism is reduced to what we are self-deceived to believe we are
being when we are actually—perhaps unconsciously—being egoistic. Any view
of human thought and action that can cut through to causes beneath conscious
motivation has teeth so long that an audience will be quick to conclude that this
is a wolf and not grandma talking to them. The visceral responses to such a view
can be potent and surprising. I know one reader of this theory who claims to have
thrown The Biology of Moral Systems (Alexander 1987) across the room at this
point. I myself admit to having written “PALTRY” in huge letters across a page
of an article when I first saw this view (Alexander 1992), by which I meant that it
destroyed morality and made it paltry. One respected speaker, whose lecture was
entirely on the subject of Alexander’s theory of self-deception, shook his head in
disgust and said from the podium, “If you can’t see what is wrong with that, I have
 Evolution and Morality } 315

nothing more to say to you”. A mere description of the theory once prompted an
otherwise kindly ex-president of a prestigious Cambridge college to shout “NO!”
and pound his fist on the table of a fancy and quiet restaurant, shaking glasses and
turning heads. Surely, if one accuses humanity of wholesale lies and posturing
precisely in place of everything heroic and generous, one should expect an uneasy
reception. Goodness is supposed to be a heavenly ideal, something to which we
can aspire with all of our being, and its behavioral counterpart rightness is born
of love, the best and purest thing this world has to offer. Yet our most explanatory
evolutionary theory insists these wonderful things to have arisen out of social con-
flict and competition, and to be saturated with manipulation, self-deception, and
the danger of being found out.
Is this the extent of the better angels of our nature? Where is the goodness that
moral philosophies and religions advertize and that we are apparently evolved to
display and encourage in others? Where does a deep-seated moral integrity fit
in this theory? The answer appears to be that it fits nowhere, or at least does not
demand a great deal of scientific explanation because we do not expect such a phe-
nomenon to be very common. We are not Homo bonus or beneficiens, but Homo
sapiens: thinking, clever, calculating, option-weighing humans. Evolutionary biol-
ogy explains the existence of the moral ideals and also explains why our motiva-
tions and behaviors do not match those ideals. In contrast, perhaps most who
discuss the biology of prosocial behavior leave us with the idea that niceness is the
norm and the rare Machiavellians are the exceptions to explain and avoid (e.g.,
de Waal 1996; Oakley 2007; Hrdy 2009; Churchland 2011). Humans do get along
remarkably well compared to a chaotic “state of nature” (Hobbes 1651), and so
the nicer perspectives do have explanatory power. The less savory parts of the
story should not be ignored, however. If Alexander and others (Batson et al. 1999;
Trivers 2000) are correct, in terms of our adherence to the ideals of the moral
point of view the goodies are the exception, if they exist at all. If there is any con-
sistent, uncalculating, and deep devotion to the moral life in actual humans, its
manifestations are odd points off the trendline, exceptions that are smoothed away
by the averaging of statistical tendency. Perhaps the most nauseating thing about
the evolutionary moral theory for the contemporary moralist is that when one
steps away from the whole picture, we can’t help but notice that despite our best
hopes and cozy thoughts, (12) we are not fundamentally good.

The biggest and least controversial shortcoming of the evolutionary account

of morality is that an explanation of morality leaves open the question, What we
are to do?—the primary moral question of the ages and (if ancient literature is
an indication) a main starting point for our curiosity about ourselves as humans.
Evolutionary biology leaves this question not only unanswered but in a way less
sensible than when we started, because its analysis has muddied the moral waters.
In fact, one who understands the evolutionary account can be forgiven for sus-
pecting that there may actually be no answer to this question in the deep sense in
316 { Human Social Evolution

which it has historically been asked; that after an iconoclastic evolutionary analy-
sis the things most vital to be said about morality and life-living have at last been
said. We are left with ethical nihilism, and so although we still need to make prac-
tical decisions, to get too excited or evangelistic about which path we take would
seem forced.
If this is the case, however, why do the ends of books and papers on the subject
of the evolution of morality remain so strongly moralistic? Take the end of “Biology
and the Moral Paradoxes,” for instance: what is the impetus for the “goal of dimin-
ishing human problems through improving self-knowledge”? And on what basis
do we consider “intergroup conflict” something that “we must supercede”? Why,
given the evolutionary function of moralizing, should we give credence to claims
that “we seek . . . world peace and world law” (all from Alexander 1982)? Moralizing
tendrils twine through Alexander’s writings, clinging to the very moral theory that
has just revealed the sordid function of moralizing. In fact, Alexander’s works deal
in increasing detail with the future of religion and hope for humanity (Alexander
2009; 2012; this volume). Values poke through the evolutionary analysis, particu-
larly at the beginnings and ends of papers, like bold weeds encroaching on a care-
fully tended garden: End mass violence and hatred of outgroups! Promote a ladder
of affluence to enfranchise all! Demand honesty in our leaders!
What is going on in these statements and encouragements, in light of the
evolutionary background? Trying to answer this question shows the difficulty of
applying or testing the hypocrisy and self-deception hypotheses in any particu-
lar case. The morals could simply be the theory at work. They could benefit the
author either by manipulating us into being more moral than the author so that
he benefits disproportionately from our group service, or else from our lauding of
his efforts. This is harsh, though exactly what the theory would claim. I do offer
this possibility tongue-in-cheek, though, since such a strategy would seem comi-
cally inauspicious right on the heels of sensitizing us to such ploys. Alternatively,
the morals promoted might approximate strategies that are actually reproduc-
tively advantageous for an individual in our current environment. In this case
the author might be behaving altruistically by giving us a heads up, contrary to
theoretical predictions—although more likely our collective appreciation of him
far outweighs his cost in letting the cat out of the bag, such that our advantage
and his own end up being in line with each other. If all of this is too cynical, a
brighter alternative is that there is wiggle room in the system, such that goodness
is not entirely something cast out as a carrot to lure donkeys into doing work for
us; and that striving after an ideal other than individual reproductive success is
actually something that some people, even after understanding the evolutionary
account, are still willing to countenance, at least to a limited extent. But lest we
be too proud, striving after such an ideal for its own sake might itself generate
a pretty nice reputation, which points us again towards the possibility of hypoc-
risy and self-deception. Thus our interpretation is plagued by an endless cyclical
regress between our behavior being captive to the evolutionary moral theory and
 Evolution and Morality } 317

rising above it. The solution to this regress may remain forever elusive. We have
no comprehensive algorithm by which to divine the impact on reproductive suc-
cess of every theory, belief, and action; and we have no intrusive psychoanalysis by
which we can discern an agent’s motivation underlying these same events. This is
not a logical or conceptual problem with Alexander’s view, as much as an inher-
ent problem (if the view is correct) in the project of humans studying themselves.
However we might choose to interpret moralizing today, one sure fact is
that morals are remarkably resilient to analysis—they survive terrible beatings.
Apparently we can’t kill the concept of goodness even when we riddle its evolution
with scandal. The concept’s very nature is to remain an unassailable ideal, regard-
less of its origins, history, or practice, and whatever the content we ascribe to it
(Murdoch 1970). We may not live the ideal, but we can’t fault it for that. Thus we
can talk about the corruption inherent in moralizing and then turn right around
and moralize with a straight face. Likewise we can bite the hand that fed us, using
our cooperative value system that was forged in group competition to bash group
competition.
There are good reasons why morals can survive the harsh treatment of an evo-
lutionary analysis. Some of these are very basic—we are moral animals, after all,
and regardless of how much we morally wander, it’s not clear that most of us are
capable of living and thinking in line with nihilism or even according to an ethic
we invent from scratch, with all due respect (i.e., very little) to postmodernists
and social constructionists. Here I will mention three other kinds of reasons—that
is, rational reasons, or rationalizations—why morals don’t completely lose face in
light of evolutionary analysis; in other words, three reasons why the last four nau-
seating elements presented above do not do morality as much damage as they may
seem to threaten, and as many people (such as those giving the visceral responses
above) have feared they would. In brief they are (1) that there is indeed a place
for the partially and even fully honest among alternative moral strategies, (2) that
self-deception means precisely that the “hypocritical” might not be hypocritical,
and (3) that the whole point of an ideal is that no amount of violation necessarily
destroys it.
First, I suggest that the few adaptive strategies so far discussed in the area of
the evolution of moral psychology need additional development. In particular, the
hypocrisy and self-deception model works as far as it goes but is too simplistic by
itself. Humans operate with varying personalities and in diverse environments and
do not always employ a uniform strategy for reproductive success, especially when
a particular strategy is risky and prone to backfire. In this area, evolutionary theo-
rists about morality should learn from salamanders and fish. In several species,
males can opt into sexual selection and compete for mates if they have the where-
withal, or else (if they do not) they can masquerade as females and gain matings
by this alternative route (Gross 1996; Brockmann 2001). If these slippery creatures
can opt for different strategies based on various individual and environmental
variables, all functioning in the same general pursuit of individual reproductive
318 { Human Social Evolution

success, one might suspect that humans can do the same in the area of coopera-
tion. A strategy of self-deception and aggrandizing one’s moral fiber, together with
the attempt to encourage more moral commitment in others than one’s own level,
comprises but a portion of a range of activities that can be adaptive in a social
context. It almost goes without saying that with our abilities of perception and dis-
crimination, behaving cooperatively in actuality, especially in the low cost situa-
tions we face every day, can be a more viable alternative than attempting to deceive
or manipulate others, especially considering the house of cards that reputation can
be, where a lifetime of cooperation can be undone with a few or even one detri-
mental act (Alexander 1987). Surely not everyone has equal powers to dissemble,
whether just to others or to oneself as well. Possibly emetics #10 and #11 above are
better seen as two common (and complementary) tools of the human trade, than
as necessarily universal and incessant practices. Of course, actually testing for the
role and importance of these psychological or subpsychological tendencies would
be more helpful than the speculation I am doing here.
Second, fish and salamanders aren’t the only things that are slippery: so are
words. When we use terms like “selfish,” “altruism,” “hypocrisy,” and “self-decep-
tion” in an evolutionary context, we do not mean precisely the same thing that we
mean by them in social usage, where these words have their ancestral currency. In
typical uses these words imply a key role for intentionality. We would never deni-
grate as “selfish” a person whose actions merely tended to benefit oneself, if the
person’s intention was to benefit someone else or to accomplish something equally
unrelated to self-benefit. Following the growth of evolutionary thought, however,
we tend to repurpose existing terms for all the new conceptual spaces that have
suddenly opened up. We now have various proximate (mechanistic, developmen-
tal) and ultimate (functional, historical) levels on which the identical terms can
be used, and the uses at the different levels are not always consistent, nor do they
always imply one another. For instance, we use “selfish” of genes as a heuristic
tool, despite the fact that genes cannot possibly have the intentionality that is typi-
cally implied by that term. We are to understand that the word is being used in a
role analogous to its typical one, despite some discontinuities, like when we say
that skies are “threatening” or that a rattling screw “wants” to come loose from a
machine. Therefore when we read “hypocrisy,” and yet admit that this phenom-
enon might not be cognitively accessible to us because we are self-deceived, what
we are really saying is that we might not really be hypocritical at all, but we might
be doing something that is analogous to hypocrisy. Real hypocrisy is presenting
an appearance of a virtuous intention that one does not really have. Hypocrisy in
the evolutionary theory of morality has a range of possibilities, including this real
hypocrisy as well as alternatives that do not actually qualify as such. One example
is a situation where one’s intention is entirely virtuous, but where that virtuous
intentionality is based partly on a series of alleles that evolved by natural selection
because that psychological state was beneficial to its bearer. Another is a situa-
tion where (at least some of) one’s conscious motivations are virtuous, but they
 Evolution and Morality } 319

are minor in their effect on action compared to certain unconscious motivations

that are self-interested and (in this case) are motivating the very same action. This
situation too would not satisfy an ordinary definition of hypocrisy because, in
this case again, one does actually have virtuous intentions. These arguments apply
equally well to “self-deception” and “altruism” (Lahti 2003): these terms in the
mouth of the evolutionary biologist are not really what they seem to be. Emetics
10 and 11 are not quite as nauseating when one takes them with this grain of salt.
Actually, the evolutionary sense of hypocrisy and self-deception leads to what
I would consider to be one of the striking paradoxes in the evolution of morality:
that “hypocrisy” and “self-deception,” in their evolutionary senses, instead of mak-
ing us worse, make us better—in fact they are our saving grace. Their importance
in the theory arises because of the possibility for inconsistency within but espe-
cially between the levels on which human behavior is controlled, the level most
relevant to morality being that of intentionality. Real hypocrisy occurs when our
intentions are inconsistent with how we represent them to others; and nearly all
of us would agree that this kind of inconsistency is generally (a bit of moralizing
now) a bad thing. But the goal of human lifetimes, insofar as we are an evolved
organism, is reproductive success. In light of that, if it were not for a similar kind
of inconsistency between levels of behavioral control, we would have exclusively
selfish intentions. In other words, if the evolutionary function of a behavior were
always manifest in our intentions, we would only be able to help others by feeling
or thinking selfishly, only care by faking it. Enter the ridiculous comment that “No
hint of genuine charity ameliorates our vision of society, once sentimentalism has
been laid aside. . . . Scratch an ‘altruist’ and watch a ‘hypocrite’ bleed” (Ghiselin 1974:
247). We can see the germ of truth in this, but it does not reflect how humans actu-
ally work. Precisely because of inconsistency between levels of control, a mother
can feed her infant with selfless love, “genuine charity,” despite the fact that the
function of her behavior is to benefit her own genetic lineage (this is considered
hypocrisy in the evolutionary analysis). And from maternal love, arguably, all love
has evolved. Love as devotion to another is only possible insofar as its psychologi-
cal workings are shielded from the adaptive basis of loving behavior; this is what
evolutionary biologists call self-deception.
Still, we must admit that our motives are impure. We cannot in good con-
science rescue good conscience solely by scapegoating some unintentional level
of behavioral control. The selfish function of behavior so regularly informs our
conscious motivations that it is likely to bleed through even when we have noble
self-impressions to the contrary. As emetic #9 above suggests, the most straight-
forward way for a genome to achieve reproductive success is simply to produce
desires and motivations that aim immediately at survival and reproduction.
Accordingly, few would disagree that desires and motivations that relate simply
and closely to survival or reproduction are among the strongest in human experi-
ence. However, our sociality often calls for a subtler route to reproductive suc-
cess (for instance, via enhancing group stability or our own reputation [Lahti &
320 { Human Social Evolution

Weinstein 2005]), in which case those basic desires and motivations may need
reining in or contravention. Even that loving mother holding an infant knows well
the mixed feelings, and consequently the need for self-control, associated with
giving so much of herself to one offspring. Some moralists and moral philosophies
demand purity of motive or intention in order for a state of mind or a behavior
to be considered good, but this situation appears to be rarely if ever actualized.
That we humans are a bundle of often inconsistent motives is a lesson delivered
not only by contemporary evolutionary psychologists (e.g., Kurzban 2010), but
frequently in the history of wise counsel on the subject. The major religions and
philosophies speak generally with one voice on this matter, thus agreeing with the
last and (to some) most frustrating of the twelve points above, that we are not as
good as we prefer to think. If we object to this point despite the history of intro-
spection and now despite evolutionary prediction, we are not necessarily fighting
for human dignity. In fact we may be revealing a defensiveness and unrealistically
high self-image. In this the demand for purity of motive resembles the demand
for free will among similarly well-meaning defenders of humanity. Most of the
argument about free will stresses the contrast between it and some sense of deter-
minism. But even if we grant a sort of agency to humans, is there any scientifically
informed person today who is really prepared to defend utterly free will? Agency
without influence? We know beyond a doubt that we have influences, both cultur-
ally acquired and inherited, and these influences sway our decisions. To demand
that there is some faculty that is somehow immune to these factors is unreason-
able. Any conception of the will that is worth considering will have to take this
diversity of interests seriously into account. In the same way, defending a moral
psychology where our motives and intentions operate in a sort of cleanroom iso-
lated from all compromising or conflictual influence is untenable and reactionary.
The spirit of the evolutionary account, and very likely literally true, is that even our
noblest attitudes and actions are moved not only by worthy but also by morally
neutral and even base influences. When I dissect my own emotional objection to
the suggestion that posturing and manipulation are an inherent part of the human
condition, I wonder how much of my objection is honest doubt as to its truth, and
how much is my wish that I and a fortiori others not be that way. I also admit an
uneasy sense, as predicted by the theory, that I don’t want open discussion of this
tendency to lead to the spread of an opinion that these strategies are acceptable.
This brings us to the third reason why morals can survive the evolutionary
account: because our own moral rectitude is not, should not be, and never really
was a condition for a functioning morality. Knowing that we are bad (to whatever
extent we are) does not wreck the ideals we hold up, or prevent us from holding
them up, any more than denying something makes it false. Nevertheless, the fact that
tendencies we would consider good evolved hopelessly tangled up with those we
would consider bad does complicate our job as moral beings. It means we are stuck
assigning moral values to attitudes and actions regardless of their original evolution-
ary function. We may praise certain things, such as sacrifice for our social group,
 Evolution and Morality } 321

and despise others, such as racism, regardless of the fact that these two tendencies
became adaptive in the context of precisely the same function: fostering group unity
in the face of competition with other groups. We do not generally consider similarity
of function to be at all a reason to assign a similar moral value, and for good reason.
In the same way, the fact that cooperation with each other and a hypocritical self-
representation both evolved for the same function has little relevance for how we
will be constructing our ideal moral values. An equally troublesome consequence
of the moral ambivalence of our history is that is that we cannot simply consult our
nature to determine how we ought to live, because the average human tendency is
not necessarily something we would want to encourage. Statistical tendency can be
important in science but does not have to be morally important to us as individual
humans. Even if psychology bears out an evolutionary prediction that the average
person’s motives are mixed, generosity is calculated, advice is self-serving, and mod-
esty is false—even if this ends up being true, whoever said that goodness had to
be the mean, had to be typical? That is the doctrine of a hopeful sort of humanist
religion we have always had plenty of reason to doubt, long before Alexander and
Trivers started talking about self-deception. The game theorists who consider nearly
all of us “good guys,” and get their papers into Science when they promise that cheats
really do lose out, owe much more to that fuzzy religion than to evolutionary biol-
ogy. Likewise those ecologists for social justice, by warning against Alexander, were
not defending society or justice so much as their own comforting conception of
human nature. Seeing ourselves as honest and caring from the core of our beings, if
this is a false view, will not help us make ourselves or the world better.
If the evolutionary account is correct about the moral ambivalence of our his-
tory and nature, we can sympathize with calls to widespread empathy (e.g., Baron-
Cohen 2011), while realizing, with Darwin, that such an idea has absolutely no
evolutionary precedent, and so must be taught (1871, ch. 4), and also realizing,
with Alexander, that bringing about such empathy will likely be arduous because
of contrary influences. If we do have widespread tendencies toward manipulation
or false moral pretenses, most likely we will be in a much better position to rectify
social ills if we are aware of these tendencies and can take them into account. This
I take to be the import of the final sentiment of the associated paper, “a society of
well-meaning people who understand themselves and their history very well is a
better milieu than a society of well-meaning people who do not.” A bigger ques-
tion is whether knowledge of the evolutionary basis of our psyche can enhance
our ability to live up to whatever ideals or goals we do espouse: take “global coop-
eration” for instance. On this point, Richard Alexander is hopeful but realistic.
In a paper he recently called his scientific swan song, he concluded by question-
ing whether the situation that started us competing in the first place—our genetic
differences, and subsequent conflicts of interest—would ever subside enough in
importance to permit peaceful coexistence as a species. As he exclaimed in the
last sentence, “If only we could devise an effective way to tackle the question—and
generate the solution—of how to make ‘otherness’ go away!” (Alexander 2012).
322 { Human Social Evolution

There are two complementary senses in which we can say that morality deals
with the ideal: The first is, as Alexander said, that the moral is never actualized
as it is conceived. The other spirit, the other side of the coin, is that the moral is
something to which we can aspire if we so choose. By engaging in such encourag-
ing words I fully admit to be falling right into Alexander’s prediction that each
individual will urge others to be more moral than oneself. Avoiding autopsycho-
analysis, if I accept for the sake of argument a degree of duplicity in my moralizing,
what is the next step? Should I abandon the whole project and be nihilistic? Or just
keep my opinions to myself? An alternative strategy is to go with the flow in just
this one area: what if I try to convince others to be better, and they try to convince
me to be better, and I like a sucker fall for them rather than steel myself with cyni-
cism. If we were to do this, society might remain a decent place to live, and might
even become more so, whereas rejecting the evolutionary account or throwing
up our hands in moral skepticism seem far less promising options. This is not
blindness to the truth, it is merely rolling with the evolutionary punches in a case
(like eating and breathing) where it is actually good for us to do so. We so often
seem to be struggling to muffle or channel recalcitrant aspects of our evolutionary
heritage; let’s just relax in this particular area and allow ourselves to moralize and
be taken in by moralizing. But of course you know there could be a devil on my
shoulder when I say that.

Acknowledgments

Many thanks to the editors for their helpful suggestions, and to Andrew Richards
for extensive input and discussion.

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 BIOLOGY AND THE MORAL PARADOXES

Alexander, R.D. Biology and the Moral Paradoxes. Journal of Biological Structures
5:389–395.

Considerations from biology suggest (1) that human interests can be generalized
as reproductive, involving activities by individuals that tend to promote the sur-
vival of their individualized sets of genes; (2) that ethical, moral and legal ques-
tions arise out of conflicts of interest that exist because of our history of genetic
differences; (3) that human behavior probably always involves egoistic tendencies
and moral inconsistency; (4) that the stages of moral development described by
social scientists correspond to the patterns of life effort discussed by biologists; (5)
that the idealized moral systems of philosophy and religion have been developed
as models that are promoted in others but not (or more than) in one’s self; and
(6) that what are usually seen as the closest approaches to these idealized models
are the sources of our most severe problems because they involve between-group
competition and strife.
Ethical, moral and legal questions arise out of conflicts of interest among
human individuals and groups. Although this assertion seems to be accepted uni-
versally, those who write on ethics, morality and law rarely emphasize it (Pound,
1941; Perry, 1954; Kelsen, 1957, represent the exceptions). Evidently, no student of
human behavior has undertaken the obvious challenge of explicitly identifying
human interests and quantifying their conflicts. Equity theory from psychology,
network and exchange theory from sociology and anthropology, and theories
of interest from law, political science and economics are partial attempts. These
theories, however, are all restricted to a superficial level, involving only reciprocal
transfers of good or beneficient acts. They neither identify the ultimate signifi-
cance of goods and beneficient acts, nor deal satisfactorily with the all-important
class of interactions that frustrated equity theorists have termed ‘deep and inti-
mate’ (Walster, Walster & Berscheid, 1978). In other words, these theories provide
no means of defining human interests in a general or complete sense, therefore, no
means of dealing generally with the intensities and directions of individual efforts
(see Alexander, 1979, and references therein).
A theory of interests is a theory of lifetimes: what they are about and how
their goals are achieved. A growing body of information and theory from
326 { Human Social Evolution

biology now provides a reasonable and testable answer: lifetimes have been molded
by natural selection to yield the greatest likelihood of survival of the individual’s
genetic materials. This likelihood is maximized by success in reproduction, which
includes producing offspring, and assisting both descendant and non-descendant
relatives. The ‘deep and intimate’ interactions causing difficulty to equity theorists
are actually those most directly involving reproduction-those occurring between
mates, potential mates and relatives. The currencies that mold the proximate
mechanisms of altruism in these interactions are genetic, not a matter of returned
goods or services, and this is the reason the payoffs have not been apparent to
investigators outside biology. Even the investments and returns of reciprocity
(exchange, equity) are ultimately comprehensible only in terms of their eventual
effects on the ‘deep and intimate’ interactions of mates and relatives. Included are
wealth, status, good will and innumerable other items.
Biologists divide lifetimes into somatic and reproductive effort: use of calories
and taking of risks in (1) building the body or soma (= amassing resources) and
(2) using the soma to reproduce (= redistributing resources in the interests of one’s
own genetic materials). Reproductive effort is in turn divisible into mating effort (on
behalf of gametes), parental effort (on behalf of offspring) and extraparental nepotis-
tic effort (on behalf of all relatives other than offspring). There are good reasons for
supposing that normal lifetimes include no other kind of effort (Alexander, 1979).
I would regard the central paradoxes of moral philosophy to be those of (1) the
incompatibility of egoism and utilitarianism (seeking the greatest benefits to one’s
self versus seeking some version of the greatest benefits to the greatest number)
and (2) the associated problem of duality in human nature. These paradoxes have
been developed and discussed in many forms, but always independently of the cur-
rent biological view of interests and life-times. I shall argue that they remain para-
doxes not because of some inherent irresolvability but because those concerned
with them have not adequately discussed the costs and benefits of either egoism
or altruism. Kalin (1968), for example, speaks of ‘winning’ and ‘coming out on top’,
and Frankena (1973, 1981) of getting ‘the best score’, but neither describes the actual
currency involved. Some authors speak of survival, but it is unlikely that humans
or any other organism have evolved to survive (Alexander, 1979), and it is easy to
show that they all do things that reduce their likelihood of survival. Essentially all
authors consider pleasure or happiness as reward (benefit) and pain and suffer-
ing as punishment (cost), but none can explain in egoistic terms either the volun-
tary acceptance of pain or the pleasure of helping others. Because the indisputable
prevalence of egoistic behavior eliminates any likelihood of a purely altruistic or
utilitarian society, except as an unattained (and as yet unexplained) pursuit or ideal,
the problem of duality, and of moral inconsistency as normal behavior, persists.
Biological theories of interests and lifetimes have the power to resolve these
paradoxes, at least in terms of the natural history of moral systems (the ‘why’ of
 Evolution and Morality } 327

behavior in respect to morality). Thus, an organism whose interests are in its own
genetic survival must first develop a soma (be a wholly or largely egoistic juvenile),
then reproduce (show the ‘altruism’ of parenthood and nepotism) while main-
taining the soma by which it continues to reproduce (thus retaining egoistic ten-
dencies during adulthood). Direct and indirect reciprocity (Alexander, 1979) are
distinctive human overlays that add to the complexity, but they create no spe-
cial problems. They may be seen as indirect somatic or nepotistic efforts routed
through pseudo- or temporarily-altruistic investments in the welfare of others
who are expected to reciprocate with interest.
The stages of moral development in the individual, as interpreted by Kohlberg
(1981) and others, are remarkably supportive of this biological view. Represented,
first, is a purely somatic (selfish, ‘amoral’) stage. This is followed by the introduc-
tion of reciprocity through a system of rewards and punishment, usually by the
parent. The individual gradually forgoes immediate rewards in favor, I would
argue, of larger later ones (reciprocity). Acceptable rewards may be both increas-
ingly later and increasingly less direct (in the senses of involving diverse curren-
cies, and of coming from society at large rather than the person or persons directly
involved in the original social act). Eventually the individual also begins to forego
personal (somatic) rewards in favor of unreciprocated rewards to others (nepo-
tism). And he becomes increasingly able to assess the profitability of social acts
without outside help.
From these arguments about interests it follows that conflicts of interest arise
out of the history of genetic differences. This hypothesis is strongly supported by
the absence of observed conflicts among non-human individuals in clones and
other cases of long-standing genetic identity, and by the general diminution of
altruism with decreasing relatedness within human societies the world over. It
explains human individuality, and bears upon powerful human issues, such as
what Wallace called ‘the impossibility, despite all the labor of God, Freud and
the Devil, of one man fully understanding another, or the loneliness of existence’
which he regarded as ‘a pan-human theme’. It explains the unique cooperative-
ness of unrelated pairs pledged to lifetime monogamy, and of genetically different
workers in the colonies of social wasps, bees, ants and termites. In both cases the
genetically different individuals involved share interests because they reproduce
through the same third parties: the offspring produced jointly by the monoga-
mous pair and the siblings of worker insects produced by their common mother. It
is significant that Kohlberg’s final stage of moral development is that in which the
individual has learned for himself how best to assess his personal costs and benefits
in following (and using) whatever social rules prevail.
Viewing humans and their moral behavior in terms of natural selection pro-
vides stark and dramatic answers to some serious and very general questions:
the incompleteness of justice; the persistence of conflicts of interest; the failure of
328 { Human Social Evolution

idealized moral systems; and the absence of universal happiness and satisfaction.
Part of the answers lie in the relative nature of success in evolutionary terms:
In natural selection the likelihood of a genetic element persisting depends
entirely on its rate of change in frequency in relation to its alternatives;
changes in absolute numbers are irrelevant. Among the attributes of living
creatures, whatever can be shown to have resulted from the action of natural
selection may be expected to bear this same relationship to its alternatives.
Thus, we should not be surprised to discover that the behavioral striving of
individual humans during history has been explicitly formed in terms of rel-
ative success in reproductive competition, that justice is necessarily incom-
plete, that happiness is not easily made universal, and that ethical questions
continue to plague us, and can even become more severe when everything
else seems to be going well. (Alexander, 1979: 240)
I stress that our interests are not individual because of genetic differences per se,
or current genetic differences, because such information has never been directly
available to humans. Relatives are known through circumstantial evidence, and only
recently have geneticists learned what the average relatedness actually is for rela-
tives whose learned assumptions about relatedness from genealogical connections
and kinds of social interactions are nevertheless usually correct. The individualized
genetic constitutions of the successions of our ancestors caused natural selection to
save and mold proximate mechanisms whereby appropriate efforts could be mounted
by individuals in each successive generation to realize their separate and individual-
ized interests. We learn who our relatives and friends are, and how to treat them; but
our learning responses are themselves evolved, and often very specific and channeled.
The hypothesis that conflicts of interest derive from the history of genetic
differences also generates new and sometimes startling questions: What are the
benefits of the group to the selfishly reproducing individual? Why does one kind of
ultrasocial group (eusocial insects) achieve its greatest numbers and unity (up to
22 million) as a single nuclear family in which one individual does all of the repro-
duction while the other (humans) achieves its greatest numbers and unity (now
approaching one billion in China) by leveling the reproductive success and oppor-
tunities of its members (through socially-imposed monogamy, graduated income
taxes, gradations of negative correlations of government support with family size,
restrictions on ‘free’ enterprise etc)? How do these questions relate to the morality
of individuals and the idealized moral systems discussed by moral philosophers?
The altruism of human nepotism and reciprocity is discriminative: Different
relatives, and relatives of different needs, are distinguished. Friends are treated
individually. As yet, no evidence of truly indiscriminate, species- or population-
wide altruism has been reported for any organism, and there is no undisputed evi-
dence for unlearned recognition of relatives in any species (Alexander, 1979). These
facts are crucial to understanding moral paradoxes and the rise of moral systems.
Indiscriminate altruism requires no special proximate mechanisms—no social
 Evolution and Morality } 329

learning. I would venture that without genetic individuality, and the consequent
discriminative altruism in nepotism and reciprocity, social learning would have
remained simple, and human society as we know it could not have evolved. The
very concepts of ethical, moral and legal would be unknown.
To think of humans existing without conflicts of interest is to assume situations
involving or mimicking group selection, in a way explicitly opposing the notion of
individuals striving to maximize their separate reproductive successes. It seems to
me that this is the ideal state of morality postulated by philosophers and social sci-
entists. If so, perhaps biology gives us the reason for understanding interpretations
such as that of Perry (1954: 100).
Morality is like a cultivated field in the midst of the desert. It is a partial and
precarious conquest. Ground that is conquered has to be protected against the
resurgence of original divisive forces. The moralized life is never immune against
demoralization. At the same time that morality gains ground in one direction it
may lose ground in another. Changes in the natural and historical environment
and the development of man himself are perpetually introducing new factors and
requiring a moral reorganization to embrace them. In the last analysis all depends
on the energy, perseverance, and perpetual vigilance of the human person.
Numerous philosophers have suggested that morality, at least as expressed in the
behavior of individuals, is in fact only an ideal, or a pursuit, and not something that
is actually realized. This idea seems consistent with the approach from evolutionary
biology that I have been describing. Thus, it is common, if not universal, to regard
morality in the behavior of an individual as consisting of a kind of altruism that yields
the altruist less than he gives. In a utilitarian system (defining utilitarianism as pro-
moting the greatest good to the greatest number) morality would not always require
that complete and indiscriminate altruism cause individual losses. This would not, for
example, be the case when the interests of the group and the interests of the individu-
als comprising the group are the same. Such a confluence of interests would happen
each time the group was threatened externally in such fashion that complete co-
operation by its members would be necessary to dissipate the threat, and when fail-
ure of the group to dissipate the threat would more severely penalize any remaining
individuals than would the use of all the individual’s effort to (successfully) support
them (this is the true, but in these times of nuclear threats forgotten, meaning of the
term ‘national security’). In other circumstances, as when some competitiveness has a
likelihood of benefiting individuals in the group (i.e. the individuals’ interests are not
all completely tied up in the survival of the group or its success in dissipating some
external threat), morality of an ideal sort would require the kind of genetic altruism,
unlikely in evolutionary terms, in which the altruist truly gets back less than he gives.
Of course, if an external threat came from another group of humans, the definition of
morality as indiscriminate altruism would again be in jeopardy.
Reflecting on these circumstances, we see that if approaches to morality are
expressed consistently, and to the degree usually achieved in society, because there
is continual pressure to bring about a condition of morality, this pressure is likely
330 { Human Social Evolution

to be applied by each individual so as to cause his neighbors, if possible, to be a

little more moral than himself. To say it another way, it would be to the advan-
tage of each individual that other individuals in his society—especially those not
closely related to him—actually achieve the ideal of completely moral behavior.
Any ideally moral person would incidentally ‘help’ every other person in the soci-
ety, however slightly, to achieve the goals that evolutionists believe have driven
evolution by natural selection, because he would hurt himself (a competitor) by
dispensing his beneficence indiscriminately. Accordingly, one might expect that
every individual in a society would gain from exerting at least a little effort toward
encouraging other individuals to be a little more moral (altruistic) than they oth-
erwise might have been. Among the many ways of furthering this aim is included
the setting up of an idealized model of morality and the encouragement of every-
one (else) to become like that. One way of promoting this outcome is to designate
as heroes (i.e. as appropriate targets for special rewards) those who most closely
approach the ideal moral condition. This line of reasoning predicts that sainthood
will be awarded to individuals who spend their lives on explicitly anti-reproduc-
tive behavior. The prevalence among saints of asceticism, self-denial, isolation
from relatives, devotion to the welfare of strangers, and otherwise indiscriminate
tendencies to be altruistic supports this hypothesis. So does the fact that sainthood
is generally awarded (long) after the death of the awardee.
So we are provided with the general hypothesis that the concept of morality,
and the establishment of systems promoting ideal moralism, at least appear to have
as their aim the support of the goals of society as a whole. For this reason, within
society, each and every individual may be expected to promote in his associates
tendencies to be moral. Because of continuing possibilities of differential success
within groups, though, we can also understand that each and every individual may
also be expected to promote a slightly greater degree of ‘morality’ (altruism) in
his neighbor than in himself. And we can understand why the idealized morality
of the philosophers is never a reality in society as a whole, and occurs only as an
accident, a manipulation or in special circumstances.
The question may be raised, why anyone should be susceptible to being manip-
ulated unduly far in the direction of morality, given that we have been subjected
to such manipulations for so long? Why, in other words, should moralizing ever
be effective?
I think there are at least four contributing factors. First, the degrees of morality
that are actually reproductively appropriate will vary dramatically as societies move
between periods of extreme danger and relative security, making it difficult to know
how to behave. When will a specified degree of failure to accede to exhortations to
be altruistic cost more than it yields, because of (1) failure of the group on which one
depends for success, or (2) responses within the group to one’s failure to be altruistic?
Second, individuals may be expected to take advantage of the dramatic shifts
in most profitable degrees of altruism to deceive others about costs or dangers so
as to induce in them unduly altruistic behavior. It is obvious that aspiring leaders
 Evolution and Morality } 331

often use such deception to promote their own leadership, as an antidote to the
supposed threat and as a promoter of unity.
Third, we may expect that the individuals in a society such as we have been
describing will evolve to deceive others about the degree of altruism they them-
selves are exhibiting: Everyone will wish to appear more altruistic than he is. There
are two reasons: This appearance, if credible, is more likely to lead to direct social
rewards than its alternatives. It is also more likely to encourage others to be more
altruistic. If one’s associates are altruistic, then he can afford to be more altruistic
than if they were not. We may expect everyone to be concerned that everyone
else appear altruistic so that people in general will feel comfortable with a higher
degree of altruism than would otherwise be the case.
Fourth, if kin recognition is learned (Alexander, 1979), mistakes are likely in
this context, and one may insinuate himself into the role of relative so as to receive
inappropriate nepotism, or even to pretend to be nepotistically altruistic so as to
receive the appropriate altruistic responses.
Playing upon the tendency of everyone to strive to appear more altruistic than
one’s self, and using the other ploys just described, may produce a considerable
amount of successful social manipulation. These various factors seem to be the
elements necessary to produce and maintain what we commonly call moral sys-
tems, and moral behavior in individuals. They represent the means for resolving
the philosophers’ paradoxes with respect to morality, and for understanding why
moral systems have always fallen short of our ideals, and why we establish and
maintain such ideals. If accurate, these arguments may also clarify the routes by
which we can most closely approach what are seen as idealized moral systems, and
perhaps most confidently avert moral disasters.
The introduction of indirect reciprocity, whereby society as a whole or some
large part of it provides the reward for altruism and the punishment for selfish-
ness, simultaneously served both society and the individuals comprising it, and
provided the vehicle for socially manipulating individuals to levels and kinds of
altruism detrimental to them (or their reproductive success). It is somewhat para-
doxical that the tendencies and pressures in the direction of idealized moral sys-
tems should serve everyone up to a point, but then be transformed by the same
forces that molded them into manipulations of the behavior of individuals that are
explicitly against their interests and in the interests of those ostensibly promoting
everyone’s interests by promoting trends toward morality in the system.
The concept of a single just God for all people, however it is believed to have
originated, implies social unity. I would regard this concept as one representation
of an idealized moral system arising out of religion; and it is just as difficult to
follow as those generated from moral philosophy. It is not trivial that the con-
cept of a single God for all people differs from that of a ‘tribal’ God looking out
for the interests of only one group or society. Adhering to this concept requires
denial of practices like slavery, caste systems and other within-group discrimina-
tion. Despite its prominence and use during times when groups are threatened
332 { Human Social Evolution

externally, the concept in some sense fails whenever such external threats involve
(or are) other groups of people. This failure is, of course, denied by the invention
of anti-Gods, or Devils, and the ascription of others’ motivations to their control.
As a US Christian picketing over the arrival of some Russians put it, ‘I could love
them if they were my enemies, but they are the enemies of God! ’
The concept of God also implies continuity of social unity—a long-lasting,
intergenerational social contract. If nepotism is our evolved function, then God
(in the sense of vex populi, vex Dei) really can guarantee a reward ‘in Heaven’, or
after our individual deaths—or a kind of ‘everlasting life’ (for our genetic materi-
als)—as a reward for moral behavior during life. This guarantee is in the form of a
renewable contract in reciprocity which occurs when those who remain after our
death use our own life of ‘morality’ to judge our children (and other relatives who
remain) as suitable risks to continue receiving (and giving, and receiving and giv-
ing, and receiving and giving . . . ) the benefits of social reciprocity. The guarantee
actually exists because, unless those in a position to honor it do so for us, the same
possibility will not exist for them. The ceremonies associated with death, and the
reverence given to the dead, are surely, in part, ritually related to this guarantee.
If morality tends to mimic the effects of group selection, if moralizing seeks
to promote this mimicry, and if tendencies for people to be altruistic are self-
reinforcing within societies, then it is not remarkable that sincere, knowledgeable
and well-meaning people sometimes resent the arguments that natural selection is
not powerful at group levels, and that humans, as individuals, have evolved to be
interested in furthering their own reproduction. Such persons may well believe (or
sense) that publicizing or stressing such arguments, even if they are correct, will
diminish altruism and morality by providing an anti-moral model. The indications
that humans have regarded moral models as extremely important in achieving
societal goals cause such a belief to be completely understandable. Nevertheless,
this attitude runs counter to the goal of diminishing human problems through
improving self-knowledge.
Our truly serious problems of morality and law stem, not from the behavior
of individuals, but from the behavior of groups that may show most dramatically
within themselves the indiscriminate altruism that represents approaches to the
idealized morality of philosophy and religion. Indeed, loyalty and patriotism are
revered as the highest forms of morality and virtue within groups. But this same
level and kind of within-group ‘morality’ has also created our most devastating
problems—those involving intergroup conflict—that we must somehow super-
cede. What we seek, when we think of world peace and world law, has no precedent
in the history of life, not to say that of humankind. There seems to be no evidence
that humans or any other organism have achieved the species-wide indiscriminate
altruism represented in the idealized moral models of philosophy and religion.
I offer only one conclusion in this brief and perhaps unsettling essay: that, in the
effort to solve humanity’s most profound problems, there is potentially great value
in adding a perspective from modern evolutionary biology to those developing
 Evolution and Morality } 333

out of philosophy, the social sciences, religion, history and the humanities. This
biological perspective must be added, not as an argument for determinism, but
precisely to the contrary, as a possible way to greater freedom, deriving from
greater knowledge of the cause-effect patterns that underlie our history and our
nature. Some of my colleagues in biology, and many people outside biology, deny
that humans can be understood in biological terms. Others cling to the notion that
we evolved by an innocuous (and hypothetical) form of group selection and can
somehow return to it. Or they argue that if this is not the case, we should deny the
truth and pretend ourselves toward world peace and human justice; or that it is
better to be ignorant with an idealized moral model before us than to know about
an immoral history. I believe that people who think in these fashions are wrong.
Worse, because of the enormity of the problems that face us, I regard approaches
that deny biology, and sometimes deny reality, as potentially deadly. Essentially
everyone thinks of himself as well-meaning, but from my viewpoint a society of
well-meaning people who understand themselves and their history very well is a
better milieu than a society of well-meaning people who do not.

Literature Cited

Alexander, R.D. 1979. Darwinism and Human Affairs. Seattle, WA: Univ. Washington Press.
Frankena, W.K. 1973. Ethics, 2nd. ed. Englewood Cliffs, NJ: Prentice Hall.
Frankena, W.K. 1980. Thinking about Morality. Ann Arbor, MI: Univ. Michigan Press.
Kalin, J. 1968. Studies in Moral Philosophy. American Philosophical Quarterly Monograph
Series, N. Rescher (ed). Oxford: Basil Blackwell.
Kelsen, H. 1957. What is justice? Justice, law, and politics in the mirror of science. Collected
essays. Berkely, CA: Univ. Calif. Press.
Kohlberg, L.L. 1981. Essays on Moral Development. I. The Philosophy of moral development.
San Francisco, CA: Harper and Row.
Perry, R.B. 1954. Realms of value: a critique of human civilization. Cambridge, MA: Harvard
Univ. Press.
Pound, R. 1941. My philosophy of law. Credos of sixteen American scholars. Boston, MA:
Boston Law Book Co.
Walster, E., G.W. Walster & E. Berscheid. 1978. Equity: Theory and Research. Boston, MA:
Allyn & Bacon, Inc.
12

Evolution and Humor

Just for fun

or the reverse.
Try falsifying this: Humor mocks reality,
social and moral reality, the kind of
reality which, in the absence of a
supernatural, necessarily has
human architects. Humor
causes human institu- -tions
to be modified, improved or destroyed, individuals
to be informed, sometimes mortified, also sometimes
destroyed, via toying with incongruities and the
ridiculous, exposing failures to comprehend
such boundaries,
functioning on
the author’s side to elevate status.
The jocular gossip
of a good-natured,
story-telling humor session makes
everyone (?) feel better and laugh
together, forming, stabilizing,
and reinforcing coalitions,
necessarily
likely to be
at least some-
what exclusive,
everyone in-
volved
 Evolution and Humor } 335

seeking
thereby to be
gainers not losers.
But contemplate falsifying this claim:
No instance of humor has ever been relished
universally: always, someone is the goat.
Alexander, 2011, p. x
This page intentionally left blank
 INTRODUCTION

The Adaptive Significance of Humor

Stan Braude

So, two orthopterists walk into a bar. . . .

The first one didn’t see it because he was busy fiddling
with his tape recorder.
The second was a former grad student following in his
advisor’s footsteps.
This old joke illustrates some of the core ideas in Alexander’s (1986) essay,
“Ostracism and indirect reciprocity: the reproductive significance of humor.” If
you did not find it humorous, keep that to yourself for now and keep reading.
Others might have found that joke humorous on a number of levels: the recogni-
tion of the joke as a variant on a familiar class of “two guys walk into a bar” jokes,
the double meaning of “walk into a bar,” the slapstick image of two people bump-
ing their heads, the allusion to Alexander being the first of the two, or to my cohort
of his former students who continue to use the methods he taught us. Alexander
(1986) offered an ultimate hypothesis of the adaptive value of jokes and humor. He
suggested that in telling jokes we elevate our status by lowering the status of others,
such as orthopterists and former graduate students. If status translates into access
to resources, he argued, it ultimately affects survival and reproduction.
In his 1986 essay, Alexander outlined an exhaustive hypothetical framework
for understanding the adaptive value of humor. However, this essay has been
cited almost exclusively for his discussion of indirect reciprocity (Dugatkin, 1998,
Hamilton and Taborsky, 2005, Killingback and Doebeli, 2002). The discussion of
humor has been mostly ignored, even by Gervais and Sloan-Wilson (2005) in their
recent Quarterly Review article on the evolution of humor. I intend to begin recti-
fying this oversight right here and now.

OSTRACIZING THE OUTGROUP OR BONDING WITH THE INGROUP?

What could be less funny than explaining a joke? Perhaps explaining all jokes?
In a parallel fashion to his habit of exhaustively laying out alternate hypotheses,
Alexander attempted to categorize all the different types of jokes. This was a key
step in testing his hypothesis that jokes are essentially ostracizing because that
338 { Human Social Evolution

model would have to fit all sorts of jokes. The model is built on the assumptions
that jokes involve breaking rules in order to trick a victim, that being tricked low-
ers the status of the victim, and that jockeying for status is a zero-sum game. While
some jokes do this explicitly and target one or few victims, others lower the sta-
tus of a whole class of individuals, and by contrast might raise the status of the
joker and his audience. Slapstick humor is an example where the status of a single
individual is lowered and ethnic jokes or those about the opposite sex demean or
ostracize larger groups.
Leacock (1938) first distinguished ostracizing humor from affiliative humor
and it has since been demonstrated experimentally that humor can enhance
group cohesion (Banning and Nelson, 1987; Greatbach and Clark, 2003; Jung,
2003; Storey, 2003; Vinton, 1989). Alexander recognized Leacock’s distinction
but pointed out that affiliative behavior can only spread by selection if affiliation
enhances survival and reproduction relative to members of other groups. Thus
he offers the distinction between jokes that are directly or indirectly ostracizing.
At first, it seems to be quite a stretch to imagine puns, clever turns of phrase, or
humorous observations on the absurdity of modern life, as ostracizing anyone,
even indirectly. But there is a much simpler and more compelling reason why all
humor is inherently ostracizing.
All humor involves recognizing a scenario and then being surprised by a twist
or unexpected ending: the punch line (Howe, 2002; Gamble, 2001; Kuhn, 1962;
Lefcourt, 2000; Ramachandran, 1998; Shulz, 1976). The ingroup in the audience
are those who get the joke. They are clearly distinguished from the outgroup who
do not get the joke, either because they do not understand the allusions or the
social context of the joke, or because they do not have sufficient mastery of the
language (Flamson and Barrett, 2008). Interestingly, demonstration that one can
express and comprehend humor in a foreign language is among the skills nec-
essary for qualifying as having the highest level of proficiency in that language
(Alderson and Huhta, 2005).
Thus all humor is inherently ostracizing because the audience is made up of
two types of people: those who get the joke, those who don’t get it, and those who
just can’t count. There could not be an ingroup without an outgroup: people who
do not see the double meaning of “walk into a bar,” do not know that Alexander
is an orthopterist, might not even know what an orthopterist is, or how former
students behave in the presence of a famous, dominant, professor.
A number of specific predictions follow from the ostracism hypothesis. Jokes
that overtly target an outgroup should elicit a hostile response (or at least a stiff
“that’s not funny”) from members of that group or their allies. On the other hand,
jokes that use special knowledge to highlight an outgroup, should elicit a very
different response by the victims (i.e., false laughter to hide the fact that you are
a member of the outgroup). This perspective on the ostracism that is inherent
in humor leads to the prediction that jokes that involve more restricted insider
information and more subtle tricks will be judged as funnier. On the other hand,
 Evolution and Humor } 339

we would expect a joke that is so obvious that anyone can recognize the scenario
and the twist would be dismissed as juvenile. Of course testing these predictions
would require finding a way to distinguish those who don’t get the joke from those
who don’t think it’s funny because we expect subjects will be reticent to admit
when they don’t get a joke. Butcher and Whissell, (1984) as well as Levy and Fenley
(1979), have used laughter as outcome data to get around some of the problems of
self-reporting.
Darwin suggested that laughter arose before smiling, but Van Hoof (1971), and
Lockard (1977) argued that the smile arose from the bared-teeth grin, while the
laugh develops from the open mouth display. Alexander (1986) discusses laugh-
ter and smiling as stages in his hypothetical scenario of the evolution of humor
and notes that although a baby’s smile is generally an attractive signal, an open
mouthed laugh is not particularly attractive. He suggests that laughing in the pres-
ence of others shows that you are not fooled by the trick that is inherent in any joke
and that you are an ally of the trickster. Similarly, the ingroup/outgroup hypoth-
esis suggests that we laugh to indicate that we are part of the ingroup that gets
the joke. In contrast, Gervais and Sloan-Wilson (2005) as well as Weisfeld (1993)
suggest that laughing only occurs in the company of others because the function
of laughter is to reinforce the joker with positive feedback, to encourage him or
her to continue entertaining us. But this proximate hypothesis offers no explana-
tion for why we would want to encourage the joker. Furthermore, if the target of
laughter as communication is the joker, and the function of laughter is to reinforce
the joker, as Gervais and Sloan-Wilson suggest, we would not expect an increase
in individual laughter in larger groups and might even predict that individuals
would be able to decrease the intensity of their laughter when the contributions of
other audience members can be pooled in signaling the joker. However, Butcher
and Whissell, (1984) as well as Levy and Fenley (1979) found that comic video
clips evoke greater laughter per person as audience size increases. If the ingroup/
outgroup hypothesis is correct, the next time you hear the orthopterist joke I sug-
gest that you laugh loud enough that everyone in the room can tell that you get all
the allusions. On the other hand, Alexander might suggest that you respond with
a groan. This not only communicates that you get the joke, but also that you think
it is just too simplistic, too obvious, or too tortured to be funny. And in the eyes of
your audience, you would raise your own status by lowering mine.

WHY DO WE ENJOY HUMOR?

Whether the ostracism is about being the butt of the joke or about being in the
group that doesn’t get the joke, we are left wondering why we enjoy humor and
actively seek it out. Alexander (1986) dismisses the problem of enjoying humor as
proximate feedback, like the pain of bumping your head into a bar. This begs the
question of what benefit anyone gains by seeking out humor. Alexander (1989)
offers the suggestion that, like art, music, literature, and theater, attending to
340 { Human Social Evolution

humor can help us develop or enhance our social-scenario building abilities that
are critical in a system of indirect reciprocity. Attending to humor may also help
us develop our sense of humor, which apparently makes us much more attrac-
tive (Bresler et al., 2005; Bressler and Balshine, 2006; Howe, 2002; Li et al., 2009;
McGee and Shevlin, 2008; Miller, 2000). Not surprisingly, “sense of humor” is a
highly rated trait on internet dating sites.
No doubt reading novels and watching theater can foster social scenario
building skills. However, the joy we experience with humor, in both social and
nonsocial settings, points to a more basic, and highly adaptive, attraction and
reward system. This system rewards us for attending to subtle abstract patterns
and surprises all around us. Alexander’s (2008) general theory of the arts sug-
gested that the common elements of “rhythm, rhyme, melody, repetition, inspira-
tion, and novelty” might be “proximate devices that cause attentiveness” (page 19
of Alexander’s supplementary footnotes). Surprisingly he does not dismiss the
importance of these proximate cues but looks for the common theme. Although
Alexander suggests that attention to these cues helps us learn to better anticipate
the future, an alternative is that they hone our ability to detect patterns and sur-
prises in the world around us. This is consistent with Levitin’s (2007) work on the
neurobiology of music.
Menon and Levitin (2005) and Blood and Zatore (2001) have shown that our
enjoyment of music comes from internal rewards in the mesolymbic system of
the brain when we recognize patterns and when our expectations are met as a
musical piece continues. Levitin (2007) further suggests that sophisticated music
requires surprising twists in the melody or chord progression. But the surprise
must still fit an unanticipated pattern (Levitin and Menon, 2005; Koelsch, et al.,
2008). Recognizing the new pattern and how it fits is rewarded, but if we cannot
recognize how the surprise fits in, the music seems discordant and unpleasant
(Blood et al., 1999; Fritz et al., 2009). At a young age and when we are musically
unsophisticated, we enjoy simple melodies and rhythms. As we gain musical expe-
rience we are able to recognize more subtle patterns and surprises, which provide
the dopamine reward and other positive feedback.
If humor and music share these common features of identifying an abstract
pattern and noticing a subtle surprise, perhaps our enjoyment of art and poetry
are also manifestations of a general reward system that hones our ever improving
skills at detecting subtle anomalies in the world around us. This general skill at
detecting a subtle discontinuity within an abstract pattern would improve with
practice and would be highly adaptive. It would make us better at tracking prey,
detecting predators and identifying deception in social situations. This hypoth-
esis might lead to the prediction that the most successful fishermen, infantry sol-
diers, poker players, or police detectives would be people who spend their leisure
time listening to music, reading poetry, or viewing sophisticated art and comedy.
Although I have not been able to uncover data with which to test these predic-
tions, Conan Doyle’s fictional detective, Sherlock Holmes, frequently spent his
 Evolution and Humor } 341

afternoons at the symphony, and Robert Parker’s Spencer and Hawk often quote
classic poetry. Nonetheless, the commonality in the underlying adaptive value of
music, humor, art, and poetry is supported by a number of brain imaging studies
that suggest a common underlying proximate mechanism.
Music, humor, and visual art all elicit marked activity of the limbic system asso-
ciated with emotion and in the dopamine reward centers in the prefrontal cortex
(Blood et al., 1999; Cella-Conde, 2004; Menon and Levitin, 2005; Mitterschiffthaler
et al., 2007; Mobbs, et al., 2002; Watson et al., 2007; Wild et al., 2003). The pre-
frontal cortex is generally associated with learning, problem solving, and puzzle
solving, but music and humor both activate more specific subregions within the
prefrontal cortex: the nucleus accumbens as well as the dorsal and ventral tegu-
mental areas. The subregions of the prefrontal cortex involved in appreciation of
visual art have not been as precisely mapped and there is no imaging data on our
response to poetry in general. However, Thierry (2008) has noted Shakespeare
used surprising word order to attract the attention of the audience or the reader
and Petterson (2004) noted that Ogden Nash’s poetry uses the devise of surprise
and incongruity in familiar scenarios.
A reward system for practicing and improving the ability to detect abstract
patterns and subtle surprising incongruities should be so fundamental that we
would expect to see evidence of it outside of humans. Like young children, Irene
Pepperberg’s parrot, Alex, clearly enjoyed the game of identifying elements of a set
that do not match. Once he mastered those games they were no longer inherently
rewarding despite the extrinsic food rewards he was offered. Alex demanded more
sophisticated games where the surprise was more and more difficult to detect
(Pepperberg, 1999). And even if Alex did not exhibit a sense of humor, McGee
(1979) suggests that apes do. He notes that gorillas and chimps that sign will laugh
after giving incongruent answers to questions and chimps will give the sign for
funny after throwing feces at people.

CONCLUSION

Alexander’s goal in writing many of the essays that have been collected in this vol-
ume was to generate an exhaustive list of alternate hypotheses and predictions in
the best Darwinian tradition and to stimulate the scientific discussion. Hence he
concluded the 1986 essay on humor, “I end this speculative essay on the note that
whether or not the particular arguments presented here are correct in any signifi-
cant way, they may support the notion that it is appropriate to examine topics like
humor in the context of evolved biological (reproductive) function.”
Although Gervais and Sloan-Wilson’s (2005) snub of Alexander (1986) might have
been a petty attempt at ostracism, it more likely results from the fact that Alexander’s
essay was published in Ethology and Sociobiology, a journal that is not indexed in
PubMed. Of the 71 articles citing Alexander 1986 (uncovered by Google Scholar),
only a handful took up Alexander’s challenge (Nesse and Lloyd, 1992; Palmer, 1993;
342 { Human Social Evolution

Polimeni and Reiss, 2006; Weisfeld, 1993) with Palmer offering the only attempt to
test of Alexander’s ostracism hypothesis in an amusing behavioral analysis of ama-
teur hockey players in Newfoundland. Nonetheless, Polimeni and Reiss demon-
strated that they were better google scholars than Gervais and Sloan-Wilson, when
they credited Alexander as “the first to methodically analyze humor and laughter
within an evolutionary context” (page 351). Perhaps the republication of this essay,
and the others in this volume, will help fulfill Alexander’s goal of provoking us to get
to work and test his hypotheses. And let’s hope that the next time two orthopterists
walk into a bar, they not only get a cold drink, but they also get the bartender’s jokes.

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 OSTRACISM AND INDIRECT RECIPROCITY

Alexander, R.D. Ostracism and Indirect Reciprocity: The Reproductive Significance

of Humor. 1986. Ethology and Sociobiology 7: 253–270.

Humor is hypothesized to be a social activity that alters the status of the

humorist positively and that of the object or victim negatively. Of the two
traditionally distingushed classes of humor, “ostracizing” humor singles
out a victim, with others present or absent either incidental affiliates of the
humorist (and one another) or unaffected. “Affiliative” humor, on the other
hand, is focused on creating or maintaining group cohesiveness, with the
identity of the victim more or less incidental.

INTRODUCTION

Cynic

A misanthrope; spec., one who believes that human conduct is motivated

wholly by self-interest.
—webster’s collegiate dictionary 1947 edition
A blackguard whose faulty vision sees things as they are, not as
they ought to be.
—ambrose bierce’s devil’s dictionary 1911 edition
In developing a topic for my contribution to this issue, I selected humor because
it is one of several attributes commonly seen as either antithetical or irrelevant to
natural selection or reproductive success (music, art, aesthetics, humor . . . ), and
committed myself explicitly to discussing it in terms of reproductive significance.
I did this for two reasons: first, I thought it would be useful to extend my efforts
toward topics likely to be most difficult to relate to evolution by natural selection;
and second, in my course on human behavior and evolution, I had already devel-
oped a fairly detailed hypothesis about humor that related it to ostracism. Indeed,
as will become clear, I unexpectedly found the analysis converging on conclusions
I had reached earlier with respect to morality (Alexander 1982, 1985, in press).
For the purposes of my discussion, I define ostracism from my 1947 edition of
Webster’s Collegiate Dictionary as “A method of temporary banishment by popu-
lar vote. . . . Exclusion by general consent from common privileges, favor, etc. [read:
resources of reproduction] . . . as, social ostracism.”
Ostracism is a topic of almost unbelievably broad significance. I see it as varying
from such extremes as shunning, excommunication, and designation of “outlaw”
346 { Human Social Evolution

to the most subtle forms of status shifting through implied or real, partial or com-
plete exclusion from temporary or even momentary and casual groupings of social
interactants. I see ostracism as an instrument for the manipulation of conflicts
and confluences of interest through adjusting access to resources. Conflicts and
confluences of interest, I believe, underlie everything that is social about humans.
What sets us apart from other organisms more than anything else seems to be (1)
the astonishing complexity of our conflicts and confluences of interest (deriving
from the fact that we continue our lives together as large groups of long-lived
adults and children mixed as relatives of varying degrees—also the reason for the
prominence and elaborateness of incest avoidance—and as accomplished social
cooperators, reciprocators, and competitors with countless ways of helping and
hurting one another); and (2) the extraordinary array of proximate mechanisms
we have evolved for assessing and dealing with our conflicts and confluences of
interest. Underlying it all, I believe (cf. Alexander 1979), is the fact that humans
achieved, apparently a very long time ago, a peculiar situation in which the great-
est threats (and aids) to individuals and groups come from other humans rather
than other species. The nature and complexity of the human psyche, I believe fur-
ther, with its aspects designated as conscious, preconscious, subconscious, and
nonconscious—as conscience, intelligence, self-awareness, foresight, and all the
rest relate powerfully to the problems of dealing appropriately with conflicts and
confluences of interest within the human social scene. Thus I see consciousness,
self-awareness, foresight, and conscience as “overrides” of more ancient and more
immediate indicators of costs and benefits (such as pain and pleasure). Humans
use consciousness, self-awareness, foresight, and conscience to estimate long-term
costs and benefits and to make decisions about rejecting short-term pleasures
or accepting short-term pains. The special condition favoring such attributes,
I hypothesize, is the ability of competing and cooperating humans to adjust con-
tinually the relationships between short and long-term costs and benefits so that
intelligence, foresight, and deliberate planning have been the best available tools
for realizing one’s own interests (for fuller discussion, see Alexander 1979, and in
press).
I have used the term “indirect reciprocity” in my title, and this also deserves
some explanation (see Alexander 1977, 1979, 1985, in press; also see Trivers 1971,
under the term “generalized reciprocity”—but not generalized reciprocity as used
by Sahlins 1965).
Direct reciprocity occurs when an individual (or a group) is beneficent toward
another and is repaid for his temporary altruism (or social investment) by a paral-
lel act of beneficence, not necessarily involving the same currency, but typically
resulting in gains for both interactants (Trivers 1971, defined this condition for-
mally and referred to it as “reciprocal altruism”).
Indirect reciprocity occurs when interested people observe direct reciproc-
ity between others and use the observations to determine who will be their own
future associates and how they will interact subsequently with the observed
 Evolution and Humor } 347

parties. Indirect reciprocity occurs whenever rewards or punishments come from

individuals or groups other than those directly involved in a social interaction
involving investment or exploitation. It includes public and private opinions, and
status. Indirect reciprocity is the foundation of moral, ethical, and legal systems.
Its existence and pervasiveness in human social life, I believe, are the most impor-
tant factors to consider in an analysis of the nature and complexity of the human
psyche. I think they account for human interest in theater in all of its guises, from
soap operas to Shakespeare, poetry to sociology, neighborhood parties to the
Olympic games. Indirect reciprocity is the reason that very few things are more
relevant to our individual social success than the ability to see ourselves as others
see us and respond appropriately (which means, I think, to cause them to see us as
we wish them to, and not otherwise).
In this article I consider the hypothesis that humor is a principle according to
which the evolved abilities and tendencies of people to see themselves as others
see them, to use ostracism to their own advantage, are manipulated so as to induce
status shifts—both subtle and not so subtle. My general hypothesis is that humor
has developed as a form of ostracism and that, historically, at least, ostracism has
tended to affect the reproduction of the ostracized individual (or group) deleteri-
ously, especially in relation to the reproduction of the ostracizers, by restricting
access to significant resources.
To my knowledge there is no well-developed previous theory of the function of
humor, in the sense of evolved or “ultimate” function, even though the literature
on humor is filled with hints in the direction I take this article. [Thus, Robinson
(1977) says that “studies . . . describe the function of humor to solidify the in-group,
to attain gratification at the expense of another group . . . ” and “There is a pecking
order to joke-telling. The joketeller is the dominant one; the joke is his weapon;
his laughter is a sign of victory. The audience is submissive; their laughter is the
sign of their acceptance of defeat.”] Absence of explicit theories of function seems
to result partly because previous authors have either attributed “function” solely
or in part to the satisfaction of some proximate system or mechanism, or because
they have avoided the question of ultimate (usually given as “survival”) function,
sometimes giving the reason that the question is not experimentally testable (for
reviews, see McGhee 1979; Schmidt and Williams 1971).
To say that a particular behavior or tendency exists or is carried out to satisfy
pleasure, relieve frustration, or even to help one deal with an immediate situation
in the sense of adjusting one’s frame of mind (e.g., gallows humor, as exemplified
by Freud’s description of the man who, on his way to the gallows on a Monday,
steps out into the sunshine and remarks, “Well, the week is beginning nicely.”)
begs the question of the reason for the existence of the effect (pleasure, relief, com-
fort) or the recognition of a mental “problem” (frustration, wrong frame of mind).
Pleasure and pain presumably exist because, respectively, they cause us to repeat
beneficial actions and avoid repeating deleterious ones (Dawkins 1976; Alexander
1979). Similarly, frustration exists, I would speculate, because of the importance of
348 { Human Social Evolution

solving problems that may be difficult. The question we have to deal with eventu-
ally, and on which I concentrate here, is precisely what such immediate mecha-
nisms are programmed to accomplish—that is, how are actions determined to be
“beneficial” and “deleterious”?
Typically we suffer pain when we incur an injury that, prior to medical tech-
nology, was reparable provided certain actions were taken and others avoided
(as in protecting an injured part). We typically do not suffer pain when injuries
irreparable prior to medical technology occur (e.g., object thrust into the brain,
damage to the spinal cord). I assume that mental pain and pleasure analogues
serve similar functions in the social scene—e.g., that the only way, in the end,
to deal with frustration and distress is to solve the problem that is causing it. In
other words, I see frustration and distress as mechanisms serving some function,
not as either incidental or pathological conditions to be relieved per se, without
connection to other difficulties. Thus, I do not use the word “function” as Flugel
(1954) used it when he said that “it seems clear that one important function of
the humorous attitude at all levels is to relieve us from the burden of reality . . . ”
(p. 713). I will argue, in the end, that the kind of humor or the aspects of humor
that in Flugel’s sense make us feel good (e.g., humor among patients in a cancer
ward) stem from group-unifying aspects of humor that originally gave us pleasure
because they cause groups to be more effective competitive units in intergroup
competition (hence, as in the cancer ward, seem to reduce some other hostile force
by providing additional motivation to deflect it).
I do not wish to underestimate the complexity of relationships between proxi-
mate and ultimate aspects of humor and its correlates, such as changes in facial
expression and laughter. Zajonc (1985) gives reasons for believing from physi-
ological effects that “laughing must be healthy . . . ” and Roger Masters (personal
communication) has similarly reminded me of the saying that “laughter is the
best medicine,” adding: “Laughter, as a predictable consequence of humor, has a
physiological effect on the organism [see also Cousins 1979]. We know that agonic
emotional states inhibit learning . . . and . . . fear is generally associated with both
subordinate status and ineffectual coping with environmental novelty. It follows
that hedonic states of emotion have, in the absence of life-threatening situations, a
likelihood of improving reproductive success. If so, laughter could . . . be positively
reinforcing because it is associated with the effective coping behavior.”
The question one has to consider is why laughter should be healthy or have ben-
eficial effects on our physiology or behavior? If, as Zajonc and Masters suggest, the
reason is purely physiological—say, through effects on blood flow to or from the
brain—then one has to ask why we do not laugh all the time or modify the involved
physiological conditions so that we experience the beneficial effects without having
to laugh. The alternative is that beneficial effects of laughter or humor, measured
as physiological, are only beneficial in social situations that evoke laughter. That is,
laughter is caused by social situations that in turn cause the laughing individual cor-
rectly to have a kind of confidence that allows concentration on things like learning
 Evolution and Humor } 349

or coping with novelty or whatever social effects accrue from hedonic feelings. In
other words, whatever the original physiological causes or effects of laughter, its
social effects must have led to feedbacks that altered the physiological effects and
associated behaviors appropriately (moreover, once humor and laughter had come
to have beneficial physiological effects, new vistas would be opened for the “enter-
tainer” who could raise his own status by creating both the social and the physi-
ological effects in situations in which they would otherwise not occur). This view
lays great emphasis on the social effects of humor and laughter, and I am convinced
that this emphasis is proper. It does not alter significantly the search for ultimate
function, which is important because it is also the ultimate shaper of the trait.

HUMOR AND STATUS

General Hypotheses
Note: I have tried to make the following set of interrelated hypotheses internally
consistent, meaning that each subhypothesis, if true, should support the main
hypothesis and, if false, deny it. I have also tried to make this set of hypotheses
exhaustive—that is, I have tried to include every situation I can think of that
involves humor. In addition I have attempted to use Darwin’s (1859) two methods
of (1) describing phenomena that, if observed, would deny my hypothesis; and (2)
analyzing observed phenomena that seem difficult to explain by my hypothesis.
The reader will see that I have not accomplished all of these goals, but perhaps my
efforts will help others who analyze humor to achieve them later.

Status Effects
I use status according to the definitions “position of affairs” or “state or condition
of a person” (Webster’s Collegiate Dictionary, 1947 ed.). My hypotheses assume
that the following are desirable (sought-after) effects on status, meaning as well
that I assume that these effects typically influence reproduction favorably by
improving access to resources:
1. Elevating of one’s own status in relation to
a. Part of the group (audience)
b. All of the group (audience)
c. One or more third parties not present
2. Lowering of someone else’s (the “victim’s”) status in relation to one’s self
a. The victim is the only individual present.
b. The victim is not the only one present.
c. The victim is not present.
3. Reinforcing (maintaining) a presumably favorable status relationship
with
a. Part of the group (audience)
b. All of the group (audience)
c. One or more third parties not present
350 { Human Social Evolution

The basic hypotheses, then, from which all those that follow are derived, are as
follows:
I. Jokes involve tricks. Trick is defined as “An artifice or strategem; crafty
procedure or practice; a cheating device” (Webster’s Collegiate Dictionary,
1947 ed.). In my opinion, dictionary definitions of cheating are unsatisfac-
tory, so I define cheating here as breaking rules or manipulating them in an
unacceptable fashion; I define rules as established procedures or contracts.
II. Tricks are devices for lowering status of those on whom they are played
and raising the status of those who play them. Telling jokes, and laughing at
them, are ways of adjusting status in one’s own favor.
III. Based on the hypothesis of ostracism or status-shifting, humor seems to
develop as two related forms:

A. Jokes that explicitly exclude or lower the status of a party or parties (by
representing a trick played successfully upon the demoted party) and
thereby also indirectly or seemingly incidentally (implicitly) bond
together those who are party to the joke (trick) or share it (e.g., ethnic,
racist, or sexist jokes).
B. Jokes that implicitly exclude or lower the status of some individual or
recognizable group by explicitly reinforcing fellowship or cohesiveness
or unity in the group (among the individuals) sharing the joke. These
include the kinds of jokes that influenced Stephen Leacock to write
that “Humor may be defined as the kindly contemplation of the
incongruities of life, and the artistic expression thereof.” (See also the
dictionary definition as “that quality which appeals to a sense of the
ludicrous or absurdly incongruous.”)
Leacock (1938) wrote in a way that anticipates (but obviously does not correspond
precisely to) the dichotomy in humor proposed here:
One is tempted to think that perhaps the original source [of humor] parted
into two streams. In one direction flowed, clear and undefiled, the humor of
human kindliness. In the other, the polluted waters of mockery and sarcasm,
the “humor” that turned to the cruel sports of rough ages, the infliction of
pain as a perverted source of pleasure, and even the rough horseplay, the
practical jokes, and the impish malice of the schoolboy. Here belongs “sar-
casm”—that scrapes the flesh of human feelings with a hoe—the sardonic
laugh . . . the sneer of the scoffer, and the snarl of the literary critic as opposed
to the kindly tolerance of the humorist.

Similarly, O’Connell (1960) stated that, following Freud, “humor’’ and “wit’’
separate into approximately the two general kinds of humor I have postulated
here, humor being associated with empathy and wit with hostility. Robinson (1977)
wrote that “Studies . . . describe the function of humor to solidify the in-group, to
 Evolution and Humor } 351

attain gratification at the expense of another group, and, more recently, as a way to
create a new image and as an agent of social change. The role of the fool in society
has been described as a means of enforcing group norms of propriety.”
Robinson also noted, tellingly, that in the medical community “the critical issue
is that it is never justifiable to make fun of or laugh at the patient or his symptoms.
Laughing with someone rarely does harm” (Robinson 1977, p. 79).
Freud (see Brill 1938), Eysenck (1947), and Flugel (1954) looked for three levels
or kinds of humor, variously termed conative (wit), affective (humor), and cogni-
tive (comic). I cannot distinguish the second and third (see also below).
IV. Humor is associated with smiling and laughing. Smiling (visual)
and laughing (auditory and visual) are ways of communicating pleasure
(truthfully or deceptively). The pleasure of smiling and laughter is a social
phenomenon.

Laughing probably occurred first as a result of physical events like tickling,

which also has social significance, and which occurs in chimpanzees (at least) as
well as in humans (Darwin 1899; Yerkes and Learned 1925; Goodall 1968). Goodall
(1968, p. 258) stated that “‘Laughing’ (a series of staccato panting grunts) fre-
quently accompanied bouts of wrestling and tickling.” Goodall also noted that, in
“greeting behavior . . . as two individuals approach each other they may utter soft or
loud panting sounds . . . particularly the subordinate as it bows, crouches, or bobs.
Sometimes both the dominant and the subordinate individuals may “grin.” [See
McGhee (1979) for numerous examples from primates.] Today laughter among
humans probably occurs most frequently during social communication without
physical contact.
It is worth stressing that what we are required to explain is not only why what
we call humor causes pleasure but (especially) why special mechanisms exist for
the communication of the pleasure that derives from humor (eventually, the same
problem must be taken up with respect to grief and crying). In the case of tickling,
it seems a reasonable hypothesis that vocal and other physical responses originally
functioned (i.e., had as their evolved significance) to keep the tickler tickling. Two
curious aspects are that (1) we cannot successfully tickle ourselves [Flugel (1954)
remarked on this fact] and (2) our tendency to be ticklish renders us vulnerable
to a kind of cruelty in the form of unwanted tickling. I see this vulnerability as
paralleling the vulnerability of humans who have evolved to appreciate and use
humor that does not involve physical events like tickling to having this apprecia-
tion and sensitivity as well turned against them. Vulnerability to excessive tick-
ling, or excessive responsiveness to tickling, sometimes takes the form of being
“goosey,” meaning to be so intolerant of tickling—or even the threat of tickling—
that a word, gesture, body movement, or simply a stare can be a form of torture
and can cause a susceptible individual to do extraordinary things like leap out of
a window or injure himself in a frantic effort to escape, even when the tormentor
is some distance away.
352 { Human Social Evolution

Evolutionary Origins of Smiling and Laughter

Smiling and laughter have been postulated either to represent a “continuum of
graded intensities” (Andrew 1963; Hinde 1974) or to have different phyletic origins
(Van Hoof 1967, 1971; Lockard et al. 1977). Following the first alternative, Darwin
(1899) seemed to postulate that laughing preceded smiling, and Hayworth (1928)
agreed. Van Hoof (1971) and Lockard et al. (1977) suggested that smiling evolved
from the “silent bared-teeth submissive grimace . . . of primates, and laughing..
., from the relaxed open-mouth display . . . of play.” Both displays are known in
several primates (Macaca, Cercopithecus, Pan, Mandrillus, and Theropithecus).
Although I am inclined to agree with Darwin and Hayworth, the two alternatives
may not affect significantly the arguments presented here.

Ontogeny of the Sense of Humor

Presumably, the evolution of smiling and laughing in infants, as with many other
aspects of infant social behavior, followed the evolution of functions in smiling
among adults. In this hypothesis the infant would be enhancing its attractiveness
to those responsible for its future by mimicking social responses that in adults
signify good will and comaraderie. The alternative hypothesis would be that smil-
ing originated as a part of the attractiveness of infants and acquired its social sig-
nificance among adults (acknowledgement of subordinance?) later, and perhaps
as a result of its significance in the parent-offspring interaction. In a sense both
hypotheses may be correct in this case. Thus, smiling may have evolved out of a
grimace associated with being tickled, and tickling may have evolved out of physi-
cal interactions between parent and offspring. As smiling acquired more profound
implications in the complex social world of adults, there may have been significant
feedback enhancing smiling and laughing in infants.
McGhee (1971) says “Grotjahn (1957) argued that the child first discovers comic
situations when he begins to master and enjoy body movements. When he begins
to feel superior to other children in this respect, he is likely to see their mistakes
or weakness as funny.” McGhee (1971) reported that “While speech mistakes and
other bumbling errors (e.g., slipping on a banana peel) are funny in their own right
to the healthy child, they may become the source of cruel and derisive laughter in
the child who feels unloved or unsure of himself.” Leuba (1941) noted that if a play-
ful attack (e.g., of tickling) becomes too serious, laughter in younger children turns
into expressions of fear. Wolff et al. (1934) similarly stated that “A child, for instance,
who has made a remark which because of its naive cleverness evokes laughter may
burst into tears if the mirth is too openly expressed.” Jones (1926) stated that the
same stimuli might arouse laughter in 16–36-month-old children on one occa-
sion but crying in another. Justin (1932) found that only incongruity “was found
to increase in its effectiveness in producing laughter as a function of age” (among
surprise or deflated expectation, superiority and degradation, incongruity and con-
trast, social smile as a stimulus, relief from strain and play situations; these did not
change during ages 3, 4, 5, 6). This last finding suggests that the directly integrating
 Evolution and Humor } 353

aspect of humor, aside from the infant’s smile, appears later in development than
the directly ostracizing aspect. The other findings indicate that children have more
difficulty than adults separating the two kinds or effects of humor.
Robinson (1977) says of “mature humor” that it “signifies . . . emotional maturity
and . . . is based upon deeper life experiences and kindly, tolerant acceptance of
oneself and therefore of others.”
These remarks seem to me to integrate interestingly with Flugel’s 1954 note
that McDougall (1923) “draws attention to the aesthetically interesting fact that
smiling is beautiful, whereas laughter is ugly. Both smiling and laughter appear in
human infants at an early age, and all observers seem to agree that developmen-
tally the smile precedes the laugh.” If smiling associates with the “mature” humor
of integration and laughter with the explicitly ostracizing function of humor, then
the hypothesis is supported that smiling by infants without physical contact may
indeed have evolved after the integrative function of humor was established. A test
would be whether or not infants of nonhuman primates smile without physical
contact. The alternative is that laughter evolved after smiling, and the ostracizing
function of humor after the integrating function. This argument is supported by
Laing’s (1939) finding that the unusual “arouses laughter earlier than the discomfi-
ture of others, and that both precede anything which might be called ‘wit,’ which
in turn is, in its early stages, visual rather than verbal” (Flugel 1954, p. 712). Laing
supposedly found that the developmental order could be described as “absurdity,”
“slapstick,” “satire,” or “whimsey. “ But none of these words—except possibly the
first—seems to describe the integrative aspect of humor, or that associated with
smiles as opposed to laughter.

Sex Differences in Humor

The only sex differences I have found so far seem to support the general hypothesis
of ostracism. Thus, O’Connell (1960) found that men appreciate “hostile wit” more
than women do, while women prefer “nonsense humor.” Jones (1926) found that
girls smile more while boys laugh more. Laing (1939) found that “girls more often
deprecated ‘unfeeling laughter.’” It has also been argued that males tell jokes more
often than females, and that they tell more sexual jokes (for the latter, see Flugel
1954). These meager findings are consistent with the prevailing opinion that men
compete more intensely than women and that they tend to do so more frequently
in coalitions (cf. Alexander 1979; Symons 1979).

Hypothesized Stages in the Evolution of Humor

Stage 1. It becomes useful to scratch or groom oneself to remove para-

sites or for other reasons.
Stage 2. In social organisms—such as between parents and offspring,
mates, or siblings (probably in all extensively parental species)—it becomes
useful (because of kin selection) to groom relatives or mates (initially for the
same reasons as above).
354 { Human Social Evolution

Stage 3. Grooming and similar activities acquire social significance

beyond removal of parasites and other original functions. They represent
or suggest a willingness to invest in the groomed individual. Thereby they
also signify a kind of exclusivity; the implication that there is a greater or
an exclusive willingness to invest in the groomed individual rather than
in other individuals. This public willingness already implies ostracism by
defining a group with a certain relationship that includes the groomer and
the groomee—the tickler and the ticklee. If all individuals were equally
willing to invest in all other individuals this implication would not arise.
If it were not important for a relationship to be exclusive, I am saying, all
grooming would not take the forms it does. The suggestion of exclusivity
may have had its initial significance for the groomee only, but in group-
living species with complex shifts of interests, where other individuals could
observe grooming, it would very quickly acquire significance for observ-
ers as well as participants. I suggest that the intimacy and exclusiveness of
tickling and grooming interactions are why they usually cause uneasiness in
some observers (necessarily being excluded), especially when they become
intense or are long continued. [elsewhere—Alexander (in press)—I argue
that because of indirect reciprocity public aspects of nepotistic and recip-
rocal interactions are crucial in understanding their overall significance.]
Radcliffe-Brown’s (1965) discussion of the “joking relationship,” which
appears to have ritualized significance between particular kinds of relatives
in certain societies, is relevant here.
Stage 4. Special responses to grooming begin to evolve (This effect prob-
ably started earlier, but the aspects of most concern to us here would likely
become complex and significant as Stage 3, above, developed.) These aspects
could include appreciative stances, movements, or vocalizations. As such
responses evolve, there will be tendencies to try to elicit them. Tickling and
its associated laughter, squirming, and focusing by the tickler on the ticklish
spots make up one example. At this stage both grooming (and its relatives
such as tickling) and responses to grooming may begin to acquire social
significance beyond either (a) the willingness of the groomer to invest and
the groomee to accept the commitments and (b) the observation by oth-
ers of the mutual commitment. That is, the grooming (tickling, horseplay,
necking, petting, whatever) may become a game (or a deception) in which
the principal significance for one or both interactants is not to develop a
deep or long-lasting commitment to the other but to attract the attention of
observers who may be better partners in such investments. Similarly, such
interactions (as in preadults) may be primarily practice or learning experi-
ences useful in later repetitions.
It has been suggested that tickling typically involves stimulation of body areas
that would be vulnerable in combat. This suggestion is consistent with the notions
that (1) tickling is play (and play is practice), (2) tickling and laughter are parts
 Evolution and Humor } 355

of interactions involving trusted associates, and (3) tickling and laughter reassure
(e.g., Hayworth, 1928). In effect, “affiliative” humor may be derived from play, or
take its form from play. (I do not think this possible interpretation changes my
arguments, but it requires more development than I can give it here.)

Stage 5. Laughter and expressions of pleasure become liberated from the

context of physical grooming, tickling, etc.—and also from such contexts as
courtship—and begin to be expressed in other social situations. This step can
only be taken as social reciprocity becomes important as the binding cement
of sociality. That step, in turn, depends upon the organism living in social
groups composed at least of a complex mix of relatives of varying degree
and different and fluctuating reproductive potentials (hence, not uniformly
sharing interests or requiring assistance) and probably as well including sets
of nonrelatives. [See Alexander (in prep.) for a fuller justification.] As ear-
lier arguments have emphasized, there are always special reasons for such
group-living, and because group-living entails automatic expenses that must
be compensated before it can evolve, these take the form of one or another
kind of hostile force (Alexander 1974, 1979). In humans, probably from the
earliest times, these hostile forces are likely to have included other human
groups. This fifth stage may be said to represent the appearance of humor in
its modern form.

Is Humor Ever Nonostracizing?

As related above, humor is seen here as a status-altering or ostracizing form of
activity. One is tempted to ask whether, as in Leacock’s view, a sixth stage has
been achieved in which some humor has acquired a social significance that rises
loftily above the two categories here described (III A,B), both of which seem to
come off as a bit grimy and contemptible. Flugel (1954) raises essentially the same
question but does not resolve it (see also Freud, in Brill 1938; and Eysenck 1947).
In the arguments presented here the question becomes whether or not “affiliative”
actions (humor) have as their ultimate function the competitive success of the
thereby unified cooperative group as compared to other groups (or individuals).
In evolutionary terms I believe the argument can be sustained that cooperative
group-living can only evolve by increasing the reproductive success of the group
members as compared to those living alone or in other groups. The reasons are
that (1) reproductive success is relative and (2) cooperative group-living cannot be
maintained and elaborated unless all of the participants somehow improve their
reproductive success. If all group members accomplish this, then the relevant
comparison can only be between members of different groups (see also Alexander
1979, in press). This means that group cooperativeness always implies at least indi-
rect intergroup competitiveness; humans, at least, have obviously not left inter-
group interactions in this realm but placed them at center stage by making them
direct, elaborate, and continual.
356 { Human Social Evolution

Interestingly enough, especially considering another humorist’s high opinion

of humorists (Leacock, quoted earlier), Ambrose Bierce (1911) defines one word
in his Devil’s Dictionary in a way that is neither cynical nor humorous. The word
is “humorist,” which he defines as “A plague that would have softened down the
hoar austerity of Pharoah’s heart and persuaded him to dismiss Israel with his best
wishes, cat-quick.” As a contrast, especially for the purpose of this essay, the word
just before “humorist,” which is “humanity,” he defines as “The human race, col-
lectively, exclusive of the anthropoid poets.” (Bierce undoubtedly saw himself as a
humorist, as did Leacock. Even cynical humorists, evidently, do not typically enjoy
jokes on themselves.)
It is most paradoxical, at first, to imagine that which seems to bring us consid-
erable social reward and pure pleasure as unpraiseworthy. But we already know
that the paradox exists. All of us have at one time or another been filled with
mirth at an episode or story that we would not share completely and that we knew
mortified or denigrated some other, and would do more severely (too severely?)
if it were known to all. What I am hypothesizing here is that in some sense this is
true of every aspect of humor, and that not only human social structure in general
but the human psyche as well has evolved in a milieu in which subtle and complex
forms of ostracism were inevitably a principal ingredient. Elsewhere (Alexander,
in press), I argue similarly that morality and justice are concepts founded on the
idea, not of equality for all, but of ostracism and exclusivity; they represent either
gestures or convictions with respect to some kind of equality within a group, but
explicitly not beyond it and in fact for the purpose of excluding some others.
The problem in our modern, dangerous world seems to be in diminishing the
one tendency while retaining and expanding the other; Darwin (1871) recognized
and described this problem in almost the same terms as modern writers (e.g.,
Singer 1981).
I emphasize that the argument that humor is invariably either direct or indi-
rect ostracism (as opposed to being solely ostracizing in one situation and solely
integrating in the other) stands or fails on the assumptions that (1) cooperative
groups form as defenses against hostile forces and (2) human groups have for a
very long time had as their raison d’etre the existence of other competitive and
hostile groups (for references and a development of the argument, see Alexander
1979; Strate 1982).
This is not to suggest that what would typically be seen as a cynical view means
that there is no escape—no way to alter any inelegant or pain-causing activities or
attitudes of humanity. But I do mean to imply that recognizing such, when and if
they exist, has a certain likelihood of assisting in efforts toward social harmony on
grander and more nearly universal scales, perhaps through explicit and deliberate
promot ion of effects of humor that integrate and diminution of effects that ostracize.
The joking relationship is a . . . relation between two persons in which
one is by custom permitted, and, in some instances required, to tease or
 Evolution and Humor } 357

make fun of the other, who in turn is required to take no offense.

radcliffe-Brown, 1965, p. 90

Greenland Eskimos . . . resolve their quarrels by duels of laughter.

The one who gets the most laughs from the audience wins. The other,
humiliated, often goes into exile.
robinson, 1977, p. 103

Sudden glory is the passion which maketh those grimaces called

laughter.
Thomas Hobbes 1651, p: 57

Kinds of Jokes
What follows is an effort to see if different kinds of jokes in different situations
seem to suppor t or deny ideas expres sed earlier. It is not a particularly good effort
at falsification, but it may point the way to better ones.
A. Puns and shaggy dog stories are regarded as the “worst” or “lowest”
forms of humor because the trick is on the listener.
1. Puns are “worst” when told to a single person, who is obligatorily the
object of ridicule. This does not mean that the greatest status shift
will take place when a pun is told to a single individual but that it is
difficult for either individual to gain when a pun is told to a single
individual. Jokes told to single individuals typically are the kind that
lower the status of a third party not present.
2. Puns are “best” (i.e., most liked by listeners) when told to several
listening parties. The reason is that the others can laugh at the one to
whom the joke seems directed (which means as well that the joke can
serve the “integrating” or “unifying” function). This hypothesis seems
to assume that jokes involving tricks on listeners will be directed at
one member when the audience includes several individuals, and
usually not to the one with the highest prestige or the one least vul-
nerable to a downward status shift. The except ion to the second part
of the exclusion is when the joke-teller has very high status and is
explicitly trying to lower the status of the individual cur rent ly hold-
ing the highest status in the group.
B. The “best” jokes are those that seem to elevate the status of the listener
(e.g., in relation to some third party, by putting that party down). For
example, James Herriott, in a series of humorous books about his life as
a veterinarian in Scotland (e.g., Herriott 1972), has the ability to cause
the episodes of his life to appear as a series of jokes upon himself, in
358 { Human Social Evolution

which “tricks” on the other participants typically seem known only to

the readers of Herriott’s books (i.e., the “trick” is that the others are being
“observed” in their idiosyncrasies by both Herriott and his readers). The
effect is to give an impression of raising the status of the readers, and
I speculate that this is one cause for the enormous success of Herriott’s
books. On the other hand, Ben K. Green, in a series of books about his
life as a veterinarian in West Texas (e.g., Green 1971) typically portrays
himself as the clever winner of every set-to, with the other parties
getting their just due and knowing it. Even if the individual stories are
inherently funny and well-told, the overall effect on the reader is quite
different, an uneasy feeling appears, and the reader tends not to like Ben
K. Green nearly as well as he does James Herriott, who has generated
truly memorable feelings of affection among his readers. (Perhaps, as one
reader suggests, the reason for Green’s failure is that he is not as effective
as, say, Mark Twain at his cynical “against the world” best at causing the
reader to identify with him.)
C. Telling jokes on others is a way of:
1. elevating one’s own status;
2. lowering the status of the butt of the joke;
3. elevating the status of the listener by:
a. allowing him to be in the right situation to laugh;
b. lowering the status of the object of ridicule;
4. increasing camaraderie or unity by identifying the butt of the joke as
a member of an adversary group or a common object of ridicule.
D. Telling jokes on oneself is a way of:
1. trying to elevate the status of the listener so as to set up a better rela-
tionship between one’s self and the listener;
2. trying to show that one’s own status is so high that it can be lowered
without changing the basic nature of the relationships;
3. trying to channel an already existing joke on one’s self so that its
effect on one’s status is less than would otherwise be the case.
E. Laughing at jokes on oneself is a way of:
1. counteracting the effect of the trick, showing that it causes pleasure,
therefore could not be detrimental—i.e., turning the trick back on
the joke-teller (Rodney Dangerfield does not lower his status by
describing the endless ways in which he purportedly has failed to get
respect; that he does not, while pretending to, is, of course, his best
joke);
2. accepting the implicit status shift in the interests of a better future
relationship with the joke-teller or listeners (or both).
 Evolution and Humor } 359

F. Laughing at jokes in the presence of others is a way of saving status in the

situation through:
1. showing (claiming) that you recognize the trick and would never be
so naive as to be taken in the same fashion;
2. telling the joke-teller (and other listeners) that you and he (they) are
on the same side and see others (the objects of ridicule) the same
way;
3. elevating (or assuring) the joke-teller’s status in relation to you or
some others (A joke can be given as a gift to a friend—i.e., as an item
to be used by the recipient to his own advantage. In my experience
such transfers are frequently followed by the receiver of the “gift”
relating to the donor how effectively it worked.)
G. Jokes on sacred topics are a way of showing that:
I. one is extremely sophisticated (has high status) and can afford to be
unconcerned about the sacredness of the topic;
2. the sacred topic is not so important (to anyone).
H. Failing to laugh at someone else’s jokes is a way of:
1. putting down the story-teller;
2. shewing one’s own sophistication, dominance, or independence.
I. Laughing “too” hard suggests a very strong (“too” strong) effort to realize
the above functions, hence implies a feeling of low status and special
need to elevate one’s own status.
J. The ultimate putdown is to see humor in a situation, or in a joking effort,
when it is not seen by the person being put down. That person has two
choices:
1. he can laugh and pretend he “got the joke”; or
2. he can sniff and pretend that he understood the joke but did not
regard it as funny.

(Note: The above situations do not exclude circumstances in which a purveyor

of humor elevates the status of an object of his humor in relation to others in
a group, but it does seem to preclude raising of the status of an object of his
humor in relation to the humorist’s status unless the status of the others is so
lowered as to result in a net elevation of the humorist’s status. In cases that
may seem to the observer to have nothing to do with status shifts it is usually
revealing to visualize a reversal of the identities of the teller of the joke and its
object.)
Obviously if the situation is such that the status of the listener is not being
threatened in respect to the joke-teller and many others in the group, but instead
the general nature of the joke promises to elevate the listener’s status—in relation
360 { Human Social Evolution

to say, some third party or class of people—then the listener may accept the tiny
loss of status from admitting that he did not “get” the joke and reap the rewards of
being able to laugh along with everyone else at the object of ridicule.

DISCUSSION

None of the above is an argument that laughter cannot be truly pleasurable,

that humor is never sincerely funny, or that any of the above functions or out-
comes are in the conscious minds or motivations of people who tell or respond
to jokes. To contrast or oppose such proximate results of humor to its possible
reproductive significance is to muddle the relationship between functions and
the mechanisms which bring them about, It also overlooks the potential signifi-
cance of self-deception in a world in which deliberateness in deception of others
is the worst of all social transgressions, and sincerity (even what the psychologist
Donald T. Campbell calls “sincere hypocrisy”) is viewed as a noble virtue. The
question is whether or not the above outline of hypotheses tends to clarify cases of
“sincerely funny” humor as well as the kinds that some of us believe we already see
as pernicious or as serving those who actively perpetuate them and sympatheti-
cally respond to them.
This raises another issue, emphasized by the fact that people chuckle to them-
selves when alone, and also seek out cartoons and other humor to read and enjoy
in solitary, even if they do not intend to (and do not) mention these experiences
to others. Depending on the precise circumstances and consequences, this fact
may not be negative to the hypotheses discussed here. The reason is that social
success may be powerfully enhanced by adjusting one’s outcomes as a result of
social scenario-building. There is no reason to believe that humor is exempt,
and the degree to which it actually does contribute to status shifts should reflect
the degree to which it has become involved in the scenario-building. In other
words, if understanding and responding to jokes is an important kind of social
behavior, then a little practice may be useful. I would hypothesize, then, that
when laughter and humor are expressed by solitary individuals (and even when
they seem to the individual to be completely internal and personal), they are
secondary derivatives of social situations, representing scenario-building that
will have its effect in later social situations, including the indirect and antici-
pated communication of the writer or performer for an absent reader, viewer,
or interactant
I end this speculative essay on the note that whether or not the particular
arguments presented here are correct in any significant way, they may support
the notion that it is appropriate to examine topics like humor in the context
of evolved biological (reproductive) function, and that humor has an aspect of
ostracism, and of coalition formation and maintenance, and is a topic worth
careful scrutiny as we intensify our concern with the problem of peaceful
 Evolution and Humor } 361

coexistence in an ever-more dangerous world of technological sophistication

and balance-of-power races.
God works wonders when he can
Here lies a lawyer, an honest man
Gracious! The two of them buried in the same grave!
—Modified from Aye (1931)

Acknowledgements

For criticisms and assistance I am grateful to the other participants in this project
and to the members of the Human Behavior and Evolution Group at the University
of Michigan. I particularly thank Bobbi S. Low, Laura Betzig, Paul Turke, Beverly
Strassmann, and Roger Masters.

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13 }

Ecological Constraints and Human

Cooperation

People! People!
People, people, everywhere,
and not a break in sight,
they copulate and propagate,
congest with all their might.
Across the planet many starve
but too few grasp the lesson;
to our festering egos fewer humans
is an abominable suggestion.
We’re everything that matters here,
all else worldly is merely tools
for us to tweak and twist at will
while we multiply like fools.
It’s quantity, more quantity,
not quality we strive for.
More macadam! More concrete!
That’s what we’re really alive for.
But those submerged in dark despair
can take this consolation:
the trend can go only so far
in a single
o
o
o
o
generation . . .
—alexander, 2011, p. 39
 INTRODUCTION

Darwin’s Question: How Can Sterility Evolve?

Laura Betzig

DARWIN’S PROBLEM: NEUTER BEES

More than two years before his book On the Origin of Species came out, Darwin sent
a letter to his bulldog, Thomas Henry Huxley, about sterile castes. “Bees offer in
one respect by far my greatest theoretical difficulty” he admitted. Then, just short of
two months before The Origin went to press, he sent another letter to his Lord High
Chancellor in Natural Science, Charles Lyell. “I fairly struck my colours before the
case of neuter-insects,” he confessed (Burkhardt et al. 1985-, Letters 2017 and 2496).
Even before he opened his first notebook on the transmutation of species,
Darwin had considered a solution to that problem. Two years into his trip aboard
HMS Beagle, after a March, 1834 stop off the South American coast, he wrote:
“The bee could not live by itself. And in the neuter, we see an individual produced
which is not fitted for the reproduction of its kind—that highest point at which
the organization of all animals, especially the lower ones, tends—therefore such
neuters are born as much for the good of the community, as the leaf-bud is for the
tree” (Darwin 1839:262).
A quarter of a century later, Darwin devoted a whole section of his book On
the Origin of Species to the “one special difficulty” that had once seemed fatal to
his whole theory. “I allude to the neuters or sterile females in insect-communities:
for these neuters often differ widely in instinct and in structure from both the
males and fertile females, and yet, from being sterile, they cannot propagate their
kind.” His simple solution to that most serious problem, the one he’d come up with
in the Falkland Islands, was that sterility might benefit relatives. “This difficulty,
though appearing insuperable, is lessened, or, as I believe, disappears, when it is
remembered that selection may be applied to the family, as well as to the indi-
vidual, and may thus gain the desired end.” Breeders with sterile family members
flourish (Darwin 1859:236–38).
But as R. D. Alexander was among the first to point out, sterile castes are not
restricted to social insects. Members of another arthropod genus, Synalpheus—
including the snapping shrimps, S. regalis, S. filidigitus, and S. chacei—have been
considered eusocial. So have members of the vertebrate genera, Heterocephalis and
366 { Human Social Evolution

Cryptomys—including the naked mole-rat, H. glaber, and the Damaraland mole-

rat, C. damarensis (Alexander et al. 1991; Sherman et al. 1991; Sherman, this vol-
ume: compare Jarvis 1981; Duffy 1992; Duffy et al. 2000; Bennett et al. 2005).
And as Alexander and others have argued, sterile workers are not always the
close relatives of breeding queens and kings. In most cases, Darwin’s “magnifi-
cent hypothesis” holds: colony members are family members. But costs and ben-
efits also matter. Eusocial animals can be haplodiploid, diploid or clonal; many
have different mothers or fathers; some are outbred, and others are unrelated
altogether—like termites in fused groups, or cofoundress paper wasps, or slave
ants (Hölldobler and Wilson 1990; Queller et al. 2000; Korb and Schneider 2007).
Wherever the benefit-to-cost ratio is high enough, individuals should be selected
to sacrifice breeding opportunities in order to help others—regardless of relat-
edness—reproduce (Alexander et al. 1991:4 and Sherman this volume: compare
Fisher 1930; Williams and Williams 1957; Hamilton 1964).
Eusociality, or “true” sociality, always includes a reproductive division of labor
(Batra 1966; Wilson 1971). But sterility can be a matter of degree. At one end of
the sociality continuum, workers are obligately, or permanently, sterile. And at the
other end, helpers are facultatively, or temporarily, sterile, or otherwise reproduc-
tively suppressed (Sherman et al. 1995; Crespi 2005).
H. sapiens societies span that continuum—from ancient civilizations, with their
hundreds of thousands of eunuch workers; to feudal societies, with their hun-
dreds or thousands of celibate helpers; to the more egalitarian societies we lived
in as hunter-gatherers, and live in now. After writing, or history, began, roughly
5,000 years ago in the Near East, literate societies were often eusocial. Emperors
from the Atlantic to the Pacific raised hundreds of children by thousands of
women, who were protected and provided for by eunuchs, or obligately sterile
worker castes. And after around 2,000 years ago in Western Europe, aristocrats
raised dozens of children by hundreds of women, who were protected and provi-
sioned by celibates, or facultatively sterile helpers-at-the-nest. But for more than
100,000 years before history began, most people were mothers or fathers. And for
the last few hundred years, more of us have been again.

Monarchy
In the beginning, in the first histories, Saul became Israel’s first king. He was suc-
ceeded by his lyre player, David, who was reassured by his God: “I anointed you
king over Israel, and I delivered you out of the hand of Saul; and I gave you your
master’s house, and your master’s wives into your bosom” (2 Samuel 12:7). David
surrounded himself with ladies of honor and virgin companions, and fathered a
daughter and 19 named sons. He was succeeded by his son Solomon, who kept 300
concubines and 700 wives; and Solomon was succeeded by his son, Rehoboam,
who fathered 60 daughters and 28 sons.
They were protected and defended by a sterile caste. Samuel warned the people
of Israel before he anointed Saul: “He will take the best of your fields and vineyards
 Ecological Constraints and Human Cooperation } 367

and olive orchards and give them to his servants. He will take the tenth of your
grain and of your vineyards and give it to his ʱʩʸʑʱʕʩʭ,” or sarisim, or officers, or
eunuchs. And later, when he made the announcement that Solomon would be
his successor, “David assembled at Jerusalem all the officials of Israel, the officials
of the tribes, the officers of the divisions that served the king, the commanders
of thousands, the commanders of hundreds, the stewards of all the property and
cattle of the king and his sons, together with the ʱʩʸʑʱʕʩʭ,” or sarisim, or officials, or
eunuchs. The Hebrew words ʱʩʸʑʱʕ, or saris, and ʸʱʚʡʸʱʩ, or rab-saris, can be found
45 times in the Hebrew Bible, variously rendered as officer, official, eunuch and
Rabsaris, or chief eunuch, by the translators who worked for King James. Some
of those eunuchs belonged to Egyptian pharaohs; others belonged to Assyrian,
Babylonian, Persian and Hebrew kings (1 Samuel 8:14-15; 1 Chronicles 28:1; Betzig
2005, 2009a).
In China, there are huan guan, or eunuchs, on Shang Dynasty oracle bones; and
there are eunuchs in Zhou Dynasty Shi jing odes. Qin Shihuangdi, the First August
Emperor of Qin, established a eunuch agency, the Zhongchangshi; and Ming
Dynasty emperors employed 100,000 eunuchs in 12 Directorates, 4 Offices, and 8
Bureaus, who were appointed as Grand Commandants over the court at Nanjing,
or installed as Grand Defenders over provincial armies. In India, varshadharas
(or rain holders), shandhas (or effeminates), tritiya prakritis (or third genders)
and klibas (or impotents) worked under Maurya and Gupta Dynasty emperors,
as spies and harem guards. In Greece, the first HXQRXFRL or bedkeepers, worked
in private houses; but they ran the empire in Rome. Eunuchs worked under every
emperor after Caesar: Augustus, the first emperor, was attended in public by a pair
of eunuchs; and after Constantine moved the capital to Constantinople, eunuchs
worked as the emperors’ ambassadors, and commanded the imperial armies—a
spartharius headed security, a sacellarius kept the purse, a castrensis sacri palatii
worked as palace steward, a comes sacrae vestis attended the wardrobe, a comes
domorum managed the imperial estates, and a praepositus sacri cubiculi adminis-
tered the emperor’s sacred bedchamber.
Others looked after emperors’ women and children. The Caesars were provided
with women by their senators and praetorian guardsmen, and had access to thou-
sands of ancillae, or female slaves, whose children—vernae (or homebred slaves)
and liberti (or freed slaves)—filled the Familia Caesaris, or civil service. Greeks
had access to hetairai (or courtesans) and pallakai (or concubines), pornai (or
prostitutes), and douloi (or slaves)—besides their gynaikes, or wives. Sanskrit texts
from the Arthashastra, written for the Maurya emperors, to the Kamasutra, proba-
bly finished under the Gupta emperors, mention anthapuras, or harems, for thou-
sands of women, with maternity wards and dormitories for princes and princesses.
And Chinese emperors collected women from the provinces—from the 10,000
Qin Shihuangdi herded together in 270 palaces taken from the feudal rulers, to the
100,000 assembled at Yangzhou by Yangdi. Kublai Khan may have kept another
100,000 in his summer palace at Xanadu, or Shangdu: A Y chromosome linkage
368 { Human Social Evolution

found in 16 contemporary Asian populations, and in 1/200 of all late-20th-cen-

tury men, is arguably borne by male line descendants of his grandfather, Genghis
(“Golden Lineage”) Khan (Zerjal et al. 2003; Betzig 2010, 2012, 2013).

Theocracy
Roughly a generation after Jesus of Nazareth was hung on a cross, Paul of Tarsus
sent a letter to his friends in the Corinthian church. “Are you free from a wife?” he
asked. And if so, “To the unmarried and the widows I say that it is well for them to
remain single as I do”—though it was better to marry than to burn (1 Corinthians
7:8, 27). Roughly another generation later, gospel writers had Jesus tell his follow-
ers to leave their families behind, in order to follow him. “The sons of this age
marry and are given in marriage; but those who are accounted worthy to attain to
that age and to the resurrection from the dead neither marry nor are given in mar-
riage, for they cannot die anymore, because they are equal to angels and are sons
of God” (Luke 20:34–36).
Helpers-at-the-nest, they filled the medieval Church. In the first few hundred
years after Jesus was born, in the first Roman emperor’s reign, a few monachi, or
“lonely ones,” left their families and went off to live alone in the deserts. Some
of those monks were driven into the wilderness by famine; but many were the
oblates, or “offerings,” of rich parents. By the 6th century, St. Benedict had forsaken
his father’s house to found monasteries in the Italian forests, where he took in
other men’s younger sons, and asked them—in his regula monachorum, or rules
for monks—to chastise their bodies and avoid all sins of the flesh.
So the Republic of St. Peter was carried on by monogamously married, but
promiscuous, first born sons. One day in 1148 or ’49, Christine, the last heiress of
the house of Ardres, married an heir to the count of Guines, Baldwin II. She gave
him 10 sons and daughters, and her husband added a few bastards. “Because of the
intemperate tumult of his loins he was of ungovernable lust from his first adoles-
cent impulses to his old age; very young women, especially virgins, aroused him”
(Lambert of Ardres, History, 127). There were beautiful women from St Omer;
there were noble girls from Louches. Some of the 23 or more children they gave
birth to married heirs or heiresses themselves, or became knights; other spurious
issue ended up in the church.
Gregory, the Tours bishop whose Ten Books of History tell the story of the first
Frankish kings, remembered Clovis’ father as a seducer: “His private life was one
long debauch” (Gregory of Tours, History, 2.12). Charlemagne, who descended
from Clovis, had 4 known queens and 5 known concubines: Sons of his wives
inherited his empire, or raised insurrections; sons of his mistresses became abbots
or archbishops. And the Holy Roman Emperors who descended from Otto the
Great, who descended from Charlemagne, were the fathers of swarms of bas-
tards. They kept gynaecea, or women’s workshops, all over the countryside, on
hundreds of estates; and they kept ladies of pleasure in palaces from Paris, to
Aachen, to Magdeburg. Every day, 1,000 pigs and sheep, 1,000 measures of grain,
 Ecological Constraints and Human Cooperation } 369

10 wagonloads of beer, 10 wagonloads of wine, and miscellaneous chickens, eggs,

fish and produce were shipped out to Otto the Great’s itinerant court. His descen-
dants would have consumed at least as much (Betzig 1995, 2009b).

Democracy
On a June day in 1525, Martin Luther, an Augustinian monk, married Katharina
von Bora, one of 9 nuns hustled out of their Cistercian convent in a Wittenberg fish
cart. The second son of an upwardly mobile city council member, Luther insisted
that celibacy was an unnatural state: “The devil must have ordered it,” he wrote.
In an Open Letter To the Christian Nobility of the German Nation Concerning the
Reform of the Christian Estate, he argued that not one in a hundred monks looked
for a living in church. The rest had been put there by their propertied fathers. Not
every one of a nobleman’s children could become a landowner (Luther, 1520:14).
Then on a cold day in January of 1649, seven years after the royal standard
was raised at Nottingham, the House of Commons ordered the execution of King
Charles I as a “tyrant, traitor, murderer and public enemy to the good people” of
England (Rushworth, Historical Collections, 7.1418). One-hundred-forty years later,
the Bastille was stormed; and on another cold January day of 1793, “for conspiracy
against the public liberty and general safety,” the French National Convention had
King Louis XVI guillotined (Robespierre 1794). Across the Atlantic, on a warm
July day in 1776, signers of the Declaration of Independence had agreed, by then,
that it was the right of the people to alter, or to abolish, bad government.
For the more than 100,000 years before writing began, we were fairly egalitar-
ian. Hoarders and freeloaders, bullies and braggarts were looked down on: “We
refuse one who boasts,” is how a Kalahari Bushman put it (Lee 1979: 246). Most
foragers lived hand to mouth; they stored very little food, and owned only as much
as they could carry. Any kind of leadership was temporary. And most people were
monogamous, most of the time (Betzig 1986, 1997, 2012: compare Irons 1979; Flinn
and Low 1986; Low 2000).
Then after 1492, we were more egalitarian again.

DARWIN’S SOLUTION: A FIXED ABODE

Four years before he boarded the Beagle as a biologist, Darwin took up divinity
at Cambridge. He had the life of a country parson in mind. “I find I steadily have
a distant prospect of a very quiet parsonage, & I can see it even through a grove
of Palms,” he wrote home to his sister Caroline, from Botofogo Bay. “To a person
fit to take the office, the life of a Clergyman is a type of all that is respectable &
happy: & if he is a Naturalist & has the ‘Diamond Beetle’ ave Maria; I do not know
what to say,” he wrote later, from Lima, to his cousin, William Fox. In the autobi-
ography he put together toward the end of his life, Darwin remembers that, if the
phrenologists were to be trusted, he was destined to become a clergyman: “I had
the bump of Reverence developed enough for ten Priests.” But he never intended
370 { Human Social Evolution

to live without a wife. He worried about the loss of time and money, and the added
anxiety and responsibility, of having a family; as a father, he might never go up in a
balloon, or learn French. But, “My God, it is intolerable to think of spending ones
whole life, like a neuter bee, working, working, & nothing after all,” he scribbled
in a memorandum to himself (Darwin 1838, 1882:57; Burkhardt et al. 1985-, Letters
166 and 282).
Sterility, as Darwin noted in passing, seemed to be an artifact of civilized life.
Most of the “savages” he met on his Beagle trip, or had read about since, were
married, and they generally married young. As he put it, a little unkindly, in his
Descent of Man, “the greatest intemperance with savages is no reproach.” Chastity
belonged to a “very early period in the moral history of civilized man,” he thought;
and celibacy, “ranked from a remote period as a virtue,” but to him “a senseless
practice,” had come after that (Darwin 1871:96).
As Darwin knew, and R. D. Alexander agreed, cooperation is mitigated by kin-
ship. In social insects, and in other sterile castes, family members help other family
members reproduce. But kinship isn’t always enough.
As Darwin guessed, and R. D. Alexander was among many to point out, euso-
ciality is often an effect of ecological constraints. In December of 1832, a year after
he set sail out of Davenport, the Beagle’s naturalist made a few notes about the “sav-
ages” that inhabited the southernmost part of the Americas at Tierra del Fuego, in
groups with no government or chief. Three and a half decades after his ship finally
docked at Falmouth, toward the end of his 1871 book on The Descent of Man, Darwin
suggested that civilized societies required a fixed abode. “Nomadic habits, whether
over wide plains, or through the dense forests of the tropics, or along the shores of
the sea, have in every case been highly detrimental,” he wrote (Darwin 1839:234;
1871:167). Civilizations, and their sterile castes, tend to exist in saturated habitats
(Alexander 1974, 1979; Alexander et al. 1991; Sherman, this volume: compare Emlen
1982; Vehrencamp 1983; Wilson and Hölldobler 2005; Hölldobler and Wilson 2008).
Many eusocial animals live and breed in their food. Aphids feed in the galls
of trees or shrubs; Australian thrips eat in the galls of Acacia leaves; Australian
ambrosia beetles bore galleries into Eucalpytus trees; termites devour decaying
logs; snapping shrimp scavenge in the currents of coral reef sponges; mole-rats
chew into enormous tubers under arid East African landscapes (Aoki 1977; Crespi
1992; Kent and Simpson 1992; Faulkes et al. 1997; Thorne 1997; Duffy et al. 2000).
Other eusocial animals living in rich, patchy habitats learn to grow their own
food. Ants of a variety of species herd other insects, and eat “honeydew” from the
ends of their alimentary canals; other ant species sow flowering plant gardens, and
harvest fruit pulp and nectar; honeybees forage for plant nectar, but live on the
honey they store in their hives; a variety of beetles, termites and ants raise fungus;
and H. sapiens practices agriculture (Davidson 1988, Davidson et al. 2003; Mueller
et al. 1998, 2005; Seeley 1995: compare Brock et al. 2011).
Our eusociality started in the alluvial area between the Tigris and Euphrates,
on the black soil of the Nile, along Indus and Ganges tributaries, and around the
 Ecological Constraints and Human Cooperation } 371

Yellow River, or Huanghe, where people were hemmed in by the Syrian or Saharan
Deserts, and the Himalayas or Zagros Mountains (Betzig 1994, 1996, 2012). As
Robert Carneiro once famously summed up, civilizations began along rivers rich in
life, set off by mountains and deserts, where “escape in every direction” was blocked
(Carneiro 1970:375: compare Turke 1988; Strassmann and Clarke 1993; Summers
2005; Crespi 2008; and review in Hrdy 2009). Or, in the words of China’s first histo-
rian, Sima Qian, who was castrated by the Han emperor, Wudi: “The old territory of
Qin is well protected by mountains and girdled by the Yellow River, a state fenced in
on four sides. From the time of Duke Mu to that of the First Emperor, Qin had over
twenty rulers, and at all times they were leaders among the feudal lords. Surely this
was not because generation after generation they were worthy men, but because of
the strategic position they occupied” (Sima Qian, Shi ji, 6).
Our eusociality ended after Christopher Columbus discovered a New World
(Betzig 2009b, 2010). Just over 500 years ago, in August of 1492, with the back-
ing of Ferdinand and Isabella of Spain, he started the first of four trips across the
Atlantic in three ships, sailing as far as the Caribbean and the American main-
lands. Four years later, John Cabot got a commission from Henry VII of England
to seek out and discover whatever countries or islands he could find, and made it
as far as Newfoundland. Almost a century later, Sir Walter Raleigh got a charter
from Elizabeth I to set up a colony on Roanoke Island, off the Virginia coast. Then
in May of 1607, on a commission from James I, John Smith established a perma-
nent settlement on the Chesapeake Bay. There were close to 4 million people
in the United States, mostly of British descent, by the July 4th, 1776, when 56
members of the Continental Congress signed the Declaration of Independence
(Jefferson 1776). They agreed that: “We hold these truths to be self-evident,
that all men are created equal, that they are endowed by their Creator with cer-
tain unalienable Rights, that among these are Life, Liberty and the pursuit of
Happiness.—That to secure these rights, Governments are instituted among Men,
deriving their just powers from the consent of the governed,—That whenever
any Form of Government becomes destructive of these ends, it is the Right of the
People to alter or to abolish it.”

Acknowledgment

Dick Alexander introduced me to evolutionary theory, posed the question of

reproductive opportunity leveling in human societies, and for many years made it
possible for me to work in the Insect Division of the Ruthven Museums. The rest,
as they say, is history.

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Yang, H, Hurles, M.E., Robinson, E., Gerelsaikhan, T., Dashnyam, B., Mehdi, S.Q., and
Tyler-Smith, C. 2003. The genetic legacy of the Mongols. Am. J. Hum. Evol. 72:717–21.
 THE EVOLUTION OF EUSOCIALITY

Excerpt from Alexander, R.D., Noonan, K.M., and Crespi, B.J. 1991. The Evolution
of Eusociality. In: P. Sherman, J. Jarvis, and R.D. Alexander (eds), The Biology of the
Naked Mole-Rat. Princeton, NJ: Princeton University Press, pp. 3–44.
Eusociality is a remarkable topic in evolutionary biology. The term, introduced by
Michener (1969), refers to species that live in colonies of overlapping generations
in which one or a few individuals produce all the offspring and the rest serve as
functionally sterile helpers (workers, soldiers) in rearing juveniles and protecting
the colony. The wasps, bees, ants, and termites known to live this way had previ-
ously been called the “social” insects.
The recent discovery of eusociality in aphids (Aoki 1977, 1979, 1982) and naked
mole-rats (Jarvis 1981, this volume) has provided biologists with new impetus to
understand more fully the origins and selective background of this phenomenon,
which has already played a central role in the analyses of sociality in all animals
(Hamilton 1964) and, indeed, of evolution itself (Darwin 1859). These two new
instances both broaden the search for correlates of eusociality in the widely differ-
ent groups in which it has evolved independently and stimulate comparative study
of related species of insects and vertebrates with homologous behaviors verging
on eusociality (Eickwort 1981; J. L. Brown 1987; Lacey and Sherman 1991, chap. 10).
An unusual and complicated form of sociality has thus evolved independently
in four different groups, and in one, the Hymenoptera, has persisted from perhaps
a dozen independent origins (F. M. Carpenter 1953; Evans 1958; Michener 1958;
Wilson 1971). Explaining this phenomenon requires attention to a number of dif-
ferent questions. Darwin (1859) answered the basic one, How can natural selection
produce forms that would give up the opportunity to reproduce, instead using
their lives to contribute to the success of the offspring of another individual?

Darwin’s Question: How Can Sterility Evolve?

Darwin used the origin of sterile castes as a potential falsifying proposition for
his theory of evolution by natural selection. He referred to “the neuters or ster-
ile castes in insect-communities ... [which] from being sterile... cannot propagate
their kind” as “the one special difficulty, which at first appeared to me insuperable,
and actually fatal to my whole theory” (1859, p. 236). To solve the problem of how
the sterile castes could evolve, he generated the magnificent hypothesis, which still
376 { Human Social Evolution

stands, that if sterility (or any trait of a sterile form) can be carried without being
expressed, then if those who express it contribute enough to the reproduction of
others who carry the trait but do not express it, the trait itself can be “advanced
by natural selection” (p. 236). In other words, if functionally sterile individuals
help relatives produce offspring and thereby cause enough copies of the helping
tendency to be created, then the tendency (ability, potential) can spread. Darwin
was particularly concerned with how the sterile castes could evolve their own sets
of attributes; his statements indicate that when he spoke of selection at the level of
the “family” and “community” in eusocial insects, he was referring to the spread
and preservation of traits that exist among the members of groups of related indi-
viduals. Thus, in the same context, he noted that “A breed of cattle always yielding
oxen [castrates] with extraordinarily long horns could be slowly formed by care-
fully watching which individual bulls and cows, when matched, produced oxen
with the longest horns; and yet no one ox could ever have propagated its kind”
(p. 238). Similarly, he remarked that tasty vegetables could be produced by saving
seeds from relatives of the vegetables already tasted or eaten and therefore unable
to produce seeds. He also noted that cattle with “the flesh and fat . . . well marbled
together” could be bred although “the animal has been slaughtered” if “the breeder
goes . . . to the same family” (p. 238).
Darwin’s hypothesis could scarcely be improved on today, even though, not
knowing about genes, he had to rely on the concept of trait survival, and he had
no way of being quantitative. His various remarks taken together are quite close to
what modern investigators such as Hamilton (1964) and D. S. Wilson (1980) mean
when they refer, respectively, to “inclusive-fitness maximizing” and “trait-group
selection.” Darwin’s “family” method of selection to preserve traits is one of those
long advocated by agricultural scientists (e.g., Lush 1947). His remarks cited here
demonstrate the error of assertions either that Darwin invoked (a simplistic and
unsupportable kind of) group selection to explain eusociality or that he did not
discuss selection above or below the level of the individual. Darwin also showed in
these statements that he understood how organisms can carry the potential (which
we now know to be genetic) for varying their phenotypes between profoundly dif-
ferent states, depending on environmental circumstances.
Fisher (1930, p. 177) began the quantification of Darwin’s idea of reproduction
via collateral relatives (although he gave no evidence of being aware of Darwin’s
discussion when he did so) by developing a hypothesis to explain how bright col-
oration that attracted (and taught) predators could evolve in distasteful or poison-
ous caterpillars. He noted that if bright coloration were to spread among distasteful
or poisonous caterpillars traveling in sibling groups, then a caterpillar with a new
allele making it slightly more noticeable and thus more likely to give its life being
tested could thereby teach a predator to avoid the entire sibling group. But, that cat-
erpillar would have to save more than two full siblings, since each would have only
a 50% chance of carrying the same allele for brighter color. (Using phylogenetic
inference, Sillén-Tullberg [1988] argued that distastefulness and bright coloration
 Ecological Constraints and Human Cooperation } 377

often preceded gregariousness in lepidopterous larvae, but this argument does not
negate the possibility of continued exaggeration of these traits among gregarious
forms.) Fisher (1930, p. 181) also remarked that tendencies of humans to risk their
lives in heroic acts are most likely to have spread and become exaggerated because
of the beneficial effects on copies of the genes responsible located in the collection
of the hero’s relatives.
Haldane (1932) carried the arguments about reproduction via collateral rela-
tives further and also related them to the eusocial insects. (Haldane is reported
to have commented [Maynard Smith 1975; pers. comm.] that we should expect
individuals in species like our own to have evolved to give their lives only for
more than two brothers or more than eight cousins, since brothers have a one in
two chance of carrying alleles for such bravery and cousins a one in eight chance.
This comment is said by Maynard Smith to have been made sometime in the early
1950s in a pub with only Maynard Smith and Helen Spurway Haldane present [see
also Haldane 1955]. The close resemblance of this reported statement to Hamilton’s
[1964] statement has aroused some attention [see also Hamilton 1976]. In any case,
the original idea of reproduction via collateral relatives was Darwin’s, its initial
quantification was by Fisher, and, as discussed later, Hamilton [1964] first devel-
oped it extensively.) Williams and Williams (1957) discussed the evolution of euso-
cial insects, approximately in Darwin’s terms, but they were unaware of Fisher’s
discussions (G. C. Williams, pers. comm.) and added no new arguments.
Hamilton (1964) not only developed the ideas of Darwin, Fisher, and Haldane
extensively, but he also showed that maximization of what he called inclusive fit-
ness (a process some others have called kin selection, following Maynard Smith
1964) really applies to all social species. The general principle, familiar now to
nearly all biologists, is that one can reproduce not only by creating and assisting
descendants but also by assisting nondescendant or collateral relatives, and, other
things being equal, it pays more to help closer relatives than to help more distant
ones.

Literature Cited
Aoki, S. 1977. Colophinia clematis (Homoptera, Pemphigidae) an aphid species with “sol-
diers.” Kontyû 45:276–282.
Aoki, S. 1979. Further observations on Astegopteryx styracicola (Homoptera: Pemphigidae),
an aphid species with soldiers biting man. Kontyû 47:99–104.
Aoki, S. 1982. Soldiers and altruistic dispersal in aphids. In Biology of Social Insects. M.D.
Breed, C.D. Michener, and H.E. Evans, eds., pp. 154–158. Boulder, Colo.: Westview Press.
Brown, J.L. 1987. Helping and Communal Breeding in Birds. Princeton, N.J.: Princeton
University Press.
Carpenter, F.M. 1953. The geological history and evolution of insects. Am. Sci. 41:256–270.
Darwin, C.R. 1859 (1967). On the Origin of Species: a Fascimile of the First Edition and with
an Introduction by Ernst Mayr. Cambridge, Mass.: Harvard University Press.
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Eickwort, G.C. 1981. Presocial insects. In Social Insects. Vol. 2. H.R. Hermann, ed., pp. 199–
280. New York: Academic Press.
Evans, H.E. 1958. The evolution of social life in wasps. Proc. 10th Int. Congr. Entomol.
2:449–457.
Fisher, R.A. 1930. The Genetical Theory of Natural Selection. 2d. ed., 1958. New York: Dover.
Haldane, J.B.S. 1932. The Causes of Evolution. London: Longman, Green. Reprinted 1966.
Ithaca, N.Y.: Cornell University Press.
Haldane, J.B.S. 1955. Population Genetics. New Biol. 18:34–51.
Hamilton, W.D. 1964. The genetical evolution of social behavior. I, II. J. Theor. Biol. 7:1–52.
Hamilton, W.D. 1976. Haldane and altruism. New Sci. 71:40.
Jarvis, J.U.M. 1981. Eusociality in a mammal: Cooperative breeding in naked mole-rat colo-
nies. Science (Wash., D.C.) 212:571–573.
Lacey, E.A. and Sherman, P.W. 1991. Social organization of naked mole-rat colonies: evi-
dence for division of labor. In The Biology of the Naked Mole-Rat. P.W. Sherman, J.U.M.
Jarvis, R.D. Alexander, eds., pp. 274–357. Princeton, N.J.: Princeton University Press.
Lush, J.L. 1947. Family merit and individual merit as bases for selection. Am. Nat. 81:241–261.
Maynard Smith, J. 1964. Group selection and kin selection. Nature (Lond.) 201:1145–1147.
Maynard Smith, J. 1975. Survival through suicide. New Sci. 67:496–497.
Michener, C.D. 1958. The evolution of social behavior in bees. Proc. 10th Int. Congr. Entomol.
(Montreal, 1956) 2:441–447.
Michener, C.D. 1969. Comparative social behavior of bees. Annu. Rev. Entomol. 14:299–342.
Sillén-Tullberg, B. 1988. Evolution of gregariousness in aposematic butterfly larvae: a phy-
logenetic analysis. Evolution 42:293–305.
Williams, G.C. and D.C. Williams. 1957. Natural selection of individually harmful social
adaptations among sibs with special reference to social insects. Evolution 11:32–39.
Wilson, D.S. 1980. The Natural Selection of Populations and Communities. Menlo Park,
Calif.: Benjamin/Cummings.
Wilson, E.O. 1971. The Insect Societies. Cambridge, Mass.: Belknap Press of Harvard
University Press.
14 }

Evolution and Religion

God, Most Recently

To every reason for cooperating uninhibitedly,
praise the power of the Lord, our useful
and admirable metaphorical Spirit Father Figure.
Yet be conservative about passing the ammunition,
brother: genocide, though not our stated aim,
has too long been a claim to fame.
With and despite God’s existence and help,
unfortunately, we remain personally
and collectively engaged in changing
the measurements of the lifetimes
and comforts of our fellow beings in the species
that alone among the known apes of history
have gained the capability of traveling and living globally
but so far have been unable to cooperate globally
about anything at all—excepting, perhaps,
the worthiness, indeed, the seemingly shared necessity
of strong patriotism, patriotism that
continues to evolve and use its skills
and unwavering determination to destroy
every opposed and opposing side.
Asking for God’s help as our collective guiding
spirit of cooperativeness, we may convince ourselves
that we persist only toward honorable outcomes.
Sadly, it appears that we may not for some time
380 { Human Social Evolution

find ways to desist from continuing efforts

to adjust the lifetimes of our fellow humans
so frequently in the wrong direction.
—alexander, 2011, p. 295
 INTRODUCTION

The Concept of God as a Metaphor for Social Unity:

Richard Alexander’s Hypothesis
William Irons

Richard Alexander’s hypothesis about the core meaning of the concept of God is
unique among evolutionary theories of religion and performs a valuable service
to the evolutionary study of religion by focusing attention on something that most
other theories of religion have ignored. This is the question of the central values
which religion celebrates and reinforces.
There are numerous contemporary evolutionary theories of religion, but few
have focused primarily on this question, the question of how religion defines the
highest good. In a basic way, Alexander’s theory is closer to Durkheim’s (1915)
theory of religion that was put forward in the early twentieth century. Durkheim
defined religion as “a unified system of beliefs and practices related to sacred
things . . . that unite into one single moral community all those who adhere to
them” (page 62). Here the attention is clearly focused on what is valued most, and
it is the unity of the local community of close kin and neighbors which is the pri-
mary vehicle for the maximization of an individual’s inclusive fitness.
In my opinion, Alexander’s concept-of-God hypothesis needs to be expanded
to take into account how communities and societies with different social struc-
tures modify the concept of God (Wright 2009), and more importantly it needs a
complimentary theory of how religions conceive of the greatest evil. Most, if not
all, religions define not only the highest good, but also the greatest evil. Most con-
temporary theories of religion focus on one of two questions: (1) How do religious
beliefs arise? (2) What are the social consequences of religion?
The first set of theories tends to explain religion by appeal to psychological
mechanisms which cause a belief in something unseen: spirits, gods, or other
invisible agents. A good example of such a theory is the theory that religion arises
from a hyperactive agency detection device, a HADD (Dennett 2006). This has
often been explained by exploring a hypothetical but probable situation in which
evolving human beings had to decide whether they are encountering something
with agency. While sleeping in a rock shelter, a member of an early human popula-
tion might hear a noise outside the shelter that could be wind blowing branches
against the entrance to the shelter, or could be a large predator entering the shelter.
382 { Human Social Evolution

Errors in evaluating this question had very different consequences. Falsely assum-
ing it was wind when in fact it was a predator, could lead to death for oneself and
one’s family. Falsely assuming it was a predator would only lead to a restless night’s
sleep. The asymmetry of consequence favored the evolution of a psychological bias
toward ascribing agency to phenomena that were not completely understood and
might be hostile agents like predators. This bias, which is labeled a HADD, led
to the cultural evolution of beliefs in elaborate unseen agent: spirits, gods, and
so forth.
The second set of theories tends to see the consequence of religious beliefs as
enhancing social cooperation within groups. Such a benefit is usually seen as ben-
eficial to the survival of the social group and of the individual members of the
group. Logically such theories can be seen as an extension of Alexander’s earlier
theory of morality in which he argued that intergroup competition in human evo-
lution caused natural selection to favor traits that enhanced the cohesiveness of
human social groups (Alexander 1987). He pointed to morality based on indirect
reciprocity as the primary mechanism created by selection for larger and better-
united groups that would be more successful in inter-group competition. Religion
can be seen as a way of enhancing the signaling involved in indirect reciprocity.
Thus theories of this second variety tend to see religion as adaptive in ances-
tral environments and perhaps still in contemporary ones. Human beings have
evolved psychological mechanisms that cause them to invent and maintain beliefs
and rituals that unify social groups and encourage cooperation within them. The
systems of religious beliefs, rituals, and sacred stories—the religious traditions—
are complexes of interrelated memes resting on top of the evolved propensities to
absorb and practice the religion of one’s community of kith and kin. These meme
complexes also evolve as individuals find variations in them more satisfactory in
meeting the need to celebrate their most basic core value. Like other cultural insti-
tutions, they are continually changing as the members of various communities
negotiate new understandings of what means the most to them in ever-changing
circumstances of life. Thus Alexander’s concept of God hypothesis nicely comple-
ments those theories of religion which see religion as a device for forming and
maintaining cohesive social groups (Bulbulia 2004a, 2004b; Irons 2001, 2008;
Sosis, 2000, 2005; Sosis and Bressler 2003; and Wilson 2002, 2005).
Most importantly, it calls attention to the core values contained in religious
traditions—something which those studying religion from an evolutionary point
of view need to keep in mind. Being aware of the centrality of the concept of God
to the most basic values of human communities should make us appreciate why
religious beliefs are so persistent when faced by scientific challenges. This should
lead us to see the foolishness of head-on aggressive attacks on religion and suggest
instead that scientists troubled by the role of religion in discouraging acceptance
of scientific findings should seek ways to minimize the conflict between science
and literal, traditional religious beliefs.
 Evolution and Religion } 383

Alexander’s concept of God hypothesis should assume a central place in the fur-
ther development of the evolutionary study of religion. It focuses attention on a
central feature of religion which most other evolutionary theories of religion ignore.

References
Alexander, Richard D. 1987. The Biology of Moral Systems. New York: Aldine De Gruyter.
Alexander, R.D. 2011. The Mockingbird’s River Song: Poems, Essays, Songs and Stories, 1946-
2011. Manchester, MI: Woodlane Farm Books.
Bulbulia, Joseph. 2004a. Religious costs as adaptations that signal altruistic intention. Evol.
Cog. 10:19–38.
Bulbulia, Joseph. 2004b. The cognitive and evolutionary psychology of religion. Biol. Phil.
18:655–686.
Dennett, Daniel C. 2006. Breaking the Spell: Religion as a Natural Phenomenon. New York:
Viking.
Durkheim, Emile. 1915. Elementary Forms of the Religious Life. New York: Free Press.
Irons, William. 2001. Religion as a hard-to-fake sign of commitment. In: R.M. Nesse (ed.),
Evolution and the Capacity for Commitment. New York: Russell Sage Foundation,
pp. 292–309.
Irons, William. 2008. Why people believe (what some other people see as) crazy ideas, In:
J. Bulbulia, R. Sosis, E. Harris, R. Genet, C. Genet, and K. Wyman (eds.), The Evolution
of Religion: Studies, Theories, and Critiques. Santa Margarita, CA: Collins Foundation
Press.
Sosis, Richard. 2000. Religion and intragroup cooperation: preliminary results of a com-
parative analysis of utopian communities. Cross-Cult. Res. 34(1):70–87.
Sosis, Richard. 2005. Does religion promote trust? The role of signaling, reputation, and
punishment. Interdisc. J. Res. Relig. 1:1–30.
Sosis, Richard, and E. Bressler. 2003. Cooperation and commune longevity: A test of the
costly signaling theory of religion. Cross-Cult. Res. 37:211–239.
Wilson, David Sloan. 2002. Darwin’s Cathedral: Evolution, Religion, and the Nature of
Society. Chicago: University of Chicago Press.
Wilson, David Sloan. 2005. Testing major evolutionary hypotheses about religion with a
random sample. Hum. Nat. 16:382–409.
Wright, Robert. 2009. The Evolution of God. New York: Little Brown.
 RELIGION, EVOLUTION, AND THE QUEST FOR GLOBAL
HARMONY

Richard D. Alexander
(Essay original to this volume)

Introduction

This essay is an effort to bring together aspects of human existence that have pro-
ceeded more or less separately, and even antithetically. They are (1) religion, in
its principal components, and comprising the most widespread, divergent, and
tenaciously authoritative defenses of morality; (2) organic evolution, as the sci-
ence of all life; and (3) by far the most important and difficult, the effort (or at
least, a hope or desire!) to work toward world-wide social harmony. It seems to me
that the relationships of these and several other problems need to be considered
together if humans in general are to moderate their hyper-competitiveness and
hyper-patriotism, their theatrical attraction to violence, murder, and destruction,
and the world’s continuing scourge of deadly conflicts. On the one hand is the
universal and familiar coordination of personal and collective musings, beliefs,
and efforts by which humans have for centuries sought to understand themselves
and their associates; and on the other hand are the results and consequences of
the more recently recognized and analyzed process of organic evolution. To every
indication the evolutionary process has been responsible for the nature of all life,
including the scope and diversity of human sociality and the consequences of the
myriads of never-ending split-second and unexpected environmental changes
that continually modify our performances by relentlessly racing across our human
lifetimes.
The several questions I am setting out to discuss in this essay are, I think, more
difficult and more important than any others I have ever even imagined undertak-
ing. I am essentially certain that I will be unable to bring solutions to my ques-
tions together in ways that will create satisfying syntheses. But the questions are
intertwined with one another, and they might well be the most important set of
questions anyone can try to put together on almost any topic. I have started parts
of this project repeatedly, and I continue to regard my efforts as inadequate. For
example, I have tried to identify what might be termed the concept of God. But,
at least until now, my efforts (my fantasies!?) have failed to convince me that a
 Evolution and Religion } 385

universal concept of God—whether judged natural or supernatural—can ever be

applied globally, faced as we are with continuing limited or local maps of disagree-
ment that cannot serve comfortably in scatterings of differently organized parts
of the world, let alone any that can change the world as a whole. I have also tried
to think about pathways that could lead the more than seven billion people of the
world to reduce the continuing development of ever more horrendous and, almost
certainly, someday, irrevocably catastrophic weapons, and instead spread congeni-
ality and cooperation that could direct us away from the bitterness of serious com-
petitions. Of course, my thoughts about those pathways have always been less than
adequate. The size of the human population and its potential and willingness to
engage in wars and genocides seem continually to leave only hopeless discourage-
ment. But perhaps we can at least mull over the seeming inescapability of our fate.
So I am trying again. Perhaps there will be readers who can transform some of
the problems that have stymied me, and enable us all to realize what wonderful
times the world could experience if the lives of people in general could be changed
in directions of cooperativeness that over-ride their opposite competitiveness,
wars, senseless murders, and bullying. I apologize for my inadequacies, but surely
we should not be reluctant to open the doors for whatever potentially satisfying
future the people of the world may someday contemplate to build for us.

THE SCIENCE OF EVOLUTION AND ITS RECENTNESS

The three introductory topics, and questions about them, have had their begin-
nings buried in such different backgrounds, and across so many millions of years
that, despite an almost endless literature, we can scarcely imagine their specific
origins. Within the last century and a half, however, evolutionary biology has
splashed new knowledge of human social life on the scene, initially with Charles
Darwin (e.g., 1859, 1871, 1872), and subsequently with Sir Ronald A. Fisher (espe-
cially 1930, 1958), in particular discovering how the evolutionary process works
(i.e., what adaptation means, and how it takes place). Approximately a century
after Darwin, several important and broadly credible additional steps were pre-
sented (e.g., Williams and Williams 1957; Hamilton 1963–1971; Williams 1957, 1966;
Trivers 1971). And of course there has been a long-continuing explosion of an
incredibly prolific literature, some of which is referenced both directly and indi-
rectly at the end of this essay.
Unfortunately, evolution has failed to become widely accepted as the central
aspect of human understanding. Nevertheless, despite its neglect—or reluc-
tance—by humanity in general, organic evolution indisputably continues as the
universal process underlying and shaping the existence, nature, and patterning of
all forms, constituents, and divisions of life, including religious and other human
social endeavors, many of which remain unexplained. Across most or all of his-
tory, humans appear to have been largely oblivious to the workings of organic evo-
lution. Many have consistently shunned approaches to evolution, partly because
386 { Human Social Evolution

they have gained few opportunities to comprehend and use evolution to contem-
plate the adaptive processes influencing and shaping the lives of the enormous
human population. Perhaps it is also partly because many humans, especially
those who are strongly religious, simply believe that we have been getting along
just fine without assistance from a great deal of scientific knowledge (e.g., excerpts
and references from Alexander 1967–2011).

Charles Darwin’s 1859 Challenge

If it could be demonstrated that any complex organ existed, which could not
possibly have been formed by numerous, successive, slight modifications,
my theory would absolutely break down.
—on the origin of species by means of natural selection: p. 189
Despite many efforts to deny Darwin’s magnificent challenge, or declare it wrong,
it has not been dismissed or falsified across the past 152 years of its existence. In a
no-holds-barred challenge to the entire world of humanity, and with hundreds of
thousands of non-human species living in every direction, all of them presumably
available for endless testing, Darwin placed his entire theory in complete jeop-
ardy. He announced an incredible bet that, if it held, would be telling every honest
and open-minded person how to consider and identify the truth about organic
evolution—about the background of all living creatures—including humans. After
more than a century and a half without a misstep, Darwin’s daring challenge has
been demonstrated unequivocally. In the process he laid out for us the basic nature
of organisms, from genes to fertilized eggs, genomes to individuals, and including
populations predicting and describing the whole of humanity that lies before us.
Although Darwin did not generate the permanent name for what we now call
genes, he carefully and brilliantly posited precisely the requirement of “numer-
ous, successive, slight modifications,” a remarkably special set of conditions. In
1859, Darwin could not have gotten much closer to the later-arriving concept of
genes and mutations. Ironically, a packaged copy of Gregor Mendel’s paper on
the patterning of the genetics of garden peas was found on Darwin’s desk after
his death, still unopened. Mendel referred to “factors” that behaved appropriately
to Darwin’s challenge, and were also references to what would later be labeled as
“genes.” But Darwin evidently never learned about all of that, and as a result the
concept of the gene did not acquire its permanent label until around the turn of
the twentieth century.

CONCEPTS OF GOD AND THE ANTIQUITY OF RELIGION

Natural or Supernatural: Does It Make a Difference?
In this essay I suggest a possible origin, and usefulness, of the concept of God
that (1) is based on natural causes, with or without requirements matching super-
natural causes; (2) is reasonably consistent with historical and current usages,
 Evolution and Religion } 387

interpretations, and beliefs about the concept of God (there is no reason to expect
complete correspondence at this point); (3) is entirely in agreement with what we
know about the sometimes distressing outcomes of natural selection via organic
evolution; (4) is consistent with all that we know about how the human species has
evolved; and (5) proposes a concept of God as a universal entity, or spirit, that—we
can hope—is capable eventually of serving the entire human population, without
unduly restrictive ceremonies, narrowly ritualized authority, or onerous opposi-
tion to widely acceptable and reasonably fair and improvable tenets underlying
established laws and social behavior.
I suggest further that, with mindfulness, the science of evolution and the con-
cept of God may be linked to make useful contributions to acceptable versions of
the formidable question: What is the meaning of life? As well, part of the key to
reducing hostility and divisiveness among religions, and between religious and
non-religious people, may derive from active attempts to generate tolerance of
a greater acceptance and diversity in concepts of God. I have tried to make my
thoughts on these and other topics include efforts to reflect some of the similarities
and differences between religion and science, and between religion and secular-
ism, in ways that relate to the structure of this essay.
Although everything I will say here has been touched upon by countless think-
ers across a long history, not surprisingly it is difficult to locate arguments that
begin from the relatively recent process of evolutionary selection, with the conse-
quence that few combinations of arguments arrive at syntheses similar to those pre-
sented here (see references, including the appended volumes). After all, from long
before knowledge of organic evolution, the world has been filled with people who
know religion, think religion, and do so alongside most of the rest of the human
population, imbedded in many aspects of life, in practices of honesty, cooperative-
ness, congeniality, all the rest of positive sociality and comradeship; and, of course,
many less comfortable features of humanity. But formal science is not only far more
recent than is religion; much of its working is also extremely slow, compared to
the flow of rapid changes in human behavior, while, perhaps ironically, religious
morality tends to cling to constancy. The fairly recent disciplines of biology and
evolution are often misinterpreted by their connections to the long-term histories
of religions, as with, to a lesser extent, the social sciences. The significance of natu-
ral selection is often ignored or judged negatively for that reason.

***
There are at least two alternatives that may explain the nature of religion and God.
One possible alternative is that religious ceremonies and beliefs tend to be accurate
and factual, deriving from the pre-existence of a supernatural God, everlasting life,
and other special features, including the value of adhering to moral rules imposed by
authority figures accepting supernatural causes.
A second possible alternative is that religious ceremonies and beliefs have
been generated gradually and cumulatively, by straightforward expansions of the
388 { Human Social Evolution

extraordinary imagination and foresight of the human collective, or its leaders, in

the absence of anything that can legitimately be regarded as necessarily supernat-
ural, and therefore understandable as more or less metaphorical, and useful and
effective as such.
Either alternative may have been generated by people, not necessarily formally
religious, who had begun to live in organized groups for social reasons, because of
loneliness or uneasiness about proximities of neighboring aggressive or resource-
competitive groups and rising beliefs in the powers and values of willingly single or
combined authorities.
It is entirely possible that today’s various claims of religious significance have gen-
erated, survived, and persisted—indeed, thrived—because they enabled people to
succeed, especially in closely-knit groups created by adding and enhancing changes
religious in nature.
It is not difficult to find ourselves paying close attention to unusually capable
group members willing to discuss serious questions and as a result becoming leaders.
Modern human groups have little trouble identifying outstanding leaders in virtu-
ally any situation involving groups needing assistance and guidance. Such leaders are
most likely older men such as fathers or grandfathers, well known for their special
abilities (and without accounting for the curious asymmetry of access between the
sexes!). When such leaders die, it is not surprising that group members may continue
thinking about the advice they had received prior to the deceased person’s loss. Nor is
it surprising that the reputations of deceased leaders tend to grow. I suspect that virtu-
ally everyone pays special attention to the thoughts that may be passed around almost
indefinitely by group members. Offspring, grandchildren, or other close relatives of a
deceased leader may take up examples—both old and new—from a deceased leader,
and either become a new leader themselves or continue to elevate a deceased relative.
Examples may begin to derive from relatives of a deceased leader, or sometimes from
almost any members of the group. It seems likely that the more elevated the reputation
of a deceased leader, the more likely it becomes that, especially in close-knit or small
groups, the deceased leader continues to lead, by virtue of tightly-knit group actions
that elevate the deceased leader even further. How difficult should it be, then, for alert
or apprehensive group members to begin to honor their deceased leader as a Spirit or
a God? Nor is it surprising that supernaturalism can be accepted in such situations,
strengthening the wills of group members to maximize the capabilities of their group
and determining to build even further on the image of the original leader. I am sym-
pathetic, and in no way surprised, that any and all versions of God have the poten-
tial to be generated—and to be exceedingly useful—as elevated and effective leaders,
whether regarded as single or multiple, or metaphorical or supernatural, at least in the
confident minds of the seekers of peacefulness and successful group cohesion.

***
I reiterate that, despite its neglect by humans in general, and some negative
social (and other) results deriving from novel environmental effects and evolved
 Evolution and Religion } 389

consequences of gene effects, organic evolution indisputably continues as the

universal process underlying all aspects of life, including religious and all other
human social endeavors. It is scarcely plausible to assume that the increasingly
well studied and well understood human organism has little or nothing to do
with the straightforward facts of organic evolution; single organisms beginning,
as they do, from combinings of tiny and complex particles, reasonably well under-
stood through the decades of development of the human individual’s lifetime, and
including myriad expressions of social behavior across the everyday interactions
of human throngs, to finally comprehend the inexorable deterioration of the later
lives of individuals.

GROUP-LIVING: ITS REASONS AND CONSEQUENCES

If we wish to understand ourselves, across all of our history, we must eventu-

ally consider the reasons why human populations live in diverse special groups.
There is much to understand about different forms of group-living, and there have
been many efforts to describe and explain their variations (e.g., Flannery 1972;
Alexander 1979; Ember and Ember 1990; Diamond 1997; Boehm 2003, 2012, and
many others; see also the appended list of relevant books on these topics). It will
profit us to learn much about different behaviors of group members under dif-
ferent conditions of life. It will also be necessary to review the known and likely
histories of population variations, the availability and accesses of particular forms
of environments, and how group-living has changed across the centuries. These
ancient, extraordinary, and frequently changing topics have become virtually
complete journeys—indeed, complete sets of diverse journeys.
It seems almost customary to describe and explain the long period of human
distribution and social organization by starting with the earliest and least well
understood of historical questions, then working toward the present situation. It
may sometimes be more effective, however, to begin by examining the currently
existing diverse, abundant, and accessible human patterns of social life, then work
backward toward whatever can be gleaned from the necessarily less obvious, less
well understood stages from early patterns of human social life. I will attempt to
discuss a few aspects of early group-living by early humans, but I cannot provide a
detailed review of the history of human groupings across millions of years.
The kinds of group-living across the span of human history surely have been
extremely variable and distinctive, with the behavior of current groupings dramat-
ically different from the estimates of early humans. Early humans almost certainly
lived in small, separated, perhaps scattered groups, and would have been required
to be extremely cautious about predators from other species. When humans man-
aged to reduce their problems with serious large predators, as they quite obviously
have done, their groups expanded and became more mobile, and also more con-
cerned with restricting barriers, such as rivers, lakes, mountains, and other physi-
cal obstructions. Eventually, such barriers came to be crossable, allowing increased
390 { Human Social Evolution

movements and expansion of groups. Separated groups, especially those coming

from distant or different places, can be expected to view the continuing flow of
human migrants as alien or dangerous whenever they looked or acted significantly
different. Later on, barriers would have become less significant, sizes of groups
would have increased, and competition between groups, in at least some cases,
would have been more likely to treat other groups as serious adversaries or ene-
mies. Because humans have been able to reduce threats from non-human enemies,
allowing humans to attend more closely the presence of strange humans, human
groups have more or less covered the earth, and have both fought and mixed in
such ways as to live and hybridize with humans from different locations, habitats,
tribes, and other groups. Various visible or other differences among the mem-
bers of other tribes or groups created the current populations of mixed groups
and diverse nations as people moving into new locations began to live together,
producing many varieties of hybridized humans from different areas and back-
grounds. Such trends will surely continue to diminish tendencies for humans to
reject or shun individuals from other parts of the world.
The results from these rather simple suggestions have ultimately produced
what we are seeing today: crowds of diverse people, with many groups still tending
to separate themselves from other groups. Such groups have continued to overlap
extensively in regions across much of the world. It would seem that humans would
have done exactly what we might presume from our everyday observations of
appearances and performances of the people around us. It is also clear that many
or most of the different human forms, sometimes considered to be distinct species,
have been able to hybridize with groups initially from other locations. Finding
small differences in the remains of ancient anthropoids, however, is not necessarily
evidence of separate or distinct species. Nor are groups of people who suppose that
others who look or act differently, or come from distant or quite different places,
likely to represent distinct species. Our modern world demonstrates unequivo-
cally pitched battles, deadly fights, extended warring periods, and striking differ-
ences between unusual people from different locations; but this is not convincing
evidence or demonstration of evolved and completed speciation. Humans from all
over the world have come together and hybridized, producing astonishing (and
eventually comforting!) mergings of different peoples that have mingled from the
ends of the earth, and now comprise the general world population of ordinary
human beings. As a result we may be moving toward behaviors favoring global
social harmony, while nevertheless living with constant anxiety about the current
and future development of increasingly devastating weapons of war.
Today, we modern humans think mostly, I suspect, that we are simply spending
our lives in quiet, peaceful, and enjoyable social groups. It is indeed possible to
converse almost continually in many comfortable places, with congenial, friendly
people enjoying the pleasantries that surround them, and only infrequently engag-
ing in tense or serious conflicts. We tend to accept such situations almost as if they
represent the entire spectrum of human existence. Under such circumstances, for
 Evolution and Religion } 391

example, everything about wars, genocides, or murderous attacks seem far away,
sometimes even absent everywhere, especially, perhaps, in our everyday thoughts.
All too often we don’t feel a necessity to dwell upon war, or other kinds of upcom-
ing or ongoing conflict, although sometimes across long periods large numbers
of human beings just like ourselves are being slaughtered by dozens, hundreds,
thousands, or more, somewhere else. We think of ourselves as different because of
our separateness from such situations, and we mostly imagine ourselves to never
again be involved in serious negative confrontations. Many of us do indeed pass
through our lifetimes without being required to participate in military conflicts, or
without having to seek frantically to avoid the pain and deaths of innocent individ-
uals threatened by opponents, or others threatening to use the terrible devices we
humans have constructed and applied. But we continue to invent, modify, extend,
and accept new weapons in efforts to be ever more prepared to kill small or large
numbers of people, in either wars or genocides—or perhaps as attacks or defenses
against individuals and groups regarded as villainous and evil, and small groups
that continue using the same weapons created and utilized in both defense and
offense, within our own societies. We cannot rest as if what appear to be new con-
flicts will continue according to well-known strategies and changes in weaponry.
Although humans in general are scarcely aware of it, they are somewhat like
the thousands of other species that can change dramatically between different
patterns of development, quickly and definitely, in ways that fit different life pat-
terns of peaceful harmony in different environments. Unfortunately, humans have
also evolved to make incredible changes, but all too often as part of attacking and
destroying others of their own species and their own phenotypes. Our largest prob-
lem may be to eliminate that second, militant version of the human phenotype.
***

Let us understand, once and for all, that the ethical progress of society depends,
not on imitating the cosmic process, still less in running away from it, but in
combating it.
—thomas h. huxley, 1894
***
Different kinds of group-living have special significance in their relationship with
other human groups, or with individuals that do not live in groups. We might
find ourselves, in turn, in (1) small, two-generation families, (2) large families
with multiple generations and large numbers of family members, (3) mixed, out-
breeding groups—including unrelated or less closely related families that include
members of other families—and eventually (4) mixtures of large numbers of indi-
viduals among distant relatives and non-relatives. As already noted, human groups
appear at first to be peaceful cooperative members of tightly knit groups that rarely
exhibit the negative attributes listed earlier. But when members of such groups
are faced with hostile forces from other groups living relatively close by, inter-
group strife obviously can break out and result in devastating conflicts. If natural
392 { Human Social Evolution

selection tends to increase reproductive success, then we should expect to find

ways to either avoid group conflicts or else identify (not necessarily consciously)
other ways to use group conflicts to increase reproduction. This is not because we
can only function to increase reproductive success; obviously, we can consciously
reduce our own rates of reproduction. But the slow-acting, more or less uncon-
scious changes that maximize reproductive success, even without extreme com-
petitiveness and deliberate killing within our own species, may not be sufficiently
obvious to us (e.g., Chagnon 1968; Kelly 2000, 2005; Boehm 2012; Pinker 2011; and
many others).
All organisms may be expected to do whatever gives them the greatest pos-
sible advantage over other organisms that might compete with them, perhaps by
displacing or banishing them, or by seeking to destroy them. In other words, any
behaviors that disturb other organisms in ways that are sufficiently severe may
identify the winner—and the loser—thereby influencing the results of the conflict.
In these respects, humans exceed what non-human organisms can do because
humans have evolved extreme abilities for considering the future, calculating, and
pondering. They have evolved such abilities as consciousness, foresight, scenario-
building, planning, and long-term memory. Such traits have enabled humans to
increase continually their abilities to improve and expand almost every potentially
advantageous capability of importance to other humans—some traits that we all
admire and regard as our most distinctive and effective features, and others that we
rarely if ever are able to consider such features consciously. Across time, individu-
als, and later small and large groups of humans, have been able to depend on their
increasing capabilities in finding better ways to acquire food, shelter, and cloth-
ing, and to identify, improve, and learn how to create and modify weapons and
other ways to win. The human ability continually to expand understanding and
skills to overcome other organisms, and sometimes members of their own spe-
cies, has enabled humans to evolve the ability to change in directions that create
serious competitions against other members of their own species. As long as these
competitive races continue, and concentrate on group-living, situations involving
wars and their relatives may continue to become increasingly unsettled, along with
either hostile neighboring groups or, in today’s world, even distant groups. Such
differences, no matter how trivial, have often become the machineries that have
triggered, stimulated, and conducted the worst of our wars.
It is also obvious that humans, still living in groups, have expanded across vir-
tually the entire earth. During these expansions, various barriers have separated
families, clans, and other groups, often in ways that reduced or ostracized different
groups. When long periods of time separated groups, people in different groups
could differentiate, not merely in appearance, but also in their arrays of weap-
ons and competitive strategies. These different groups were sometimes composed
of people recognizable because of their historical backgrounds. Such differences
could come about because small migrating groups had diverged as results of being
isolated across lengthy periods of time.
 Evolution and Religion } 393

Why do we apply such extraordinary varieties of different terms to modes of

deliberate killings? Groups did not always combine, and, as noted earlier, were
sometimes more likely to treat the members of different groups almost as if they
represented distinct species. Examples come from such as the Europeans migrat-
ing to North America and Australia, where the immigrants believed that they had
to attack and try to destroy the American Indians and Australian Aboriginals.
Ember and Ember (1990) have estimated that 30 per cent of human males in early
groups have been killed by other males. In these and in other instances, earlier and
more distinctive or unusual inhabitants may have forced into extinction.
From early beginnings, humans have subsequently generated a virtually world-
wide variety of large and small, stable and unstable, most often overlapping popu-
lations. It is this “sea” of people that has by now exceeded more than seven billion
human individuals in the world. Such abundance of varyingly contiguous, over-
lapping, and separated populations is extremely complex in its overall structure.
Nevertheless, virtually every kind of human population now can be identified and
arranged from within the current world.
Modern people who function in groups have developed social control via
numerous organizations: governments, religions, clubs, military and administra-
tive organizations, unions, courts, teachers, farmers, businessmen, team game
players, scientists, artists, musicians, families, academies, clans, nations, kindreds,
protest groups, political societies, schools, selfish herds, and alliances of any of
these and many others. The members of such groups continually change and
divide, overlapping multiply, typically in many different arrangements. Such over-
lapping groups give opportunity for connections and cooperation of numerous
groups to respond successfully to one another, and to the collection of groups as a
unit. One result is that very large groups can be formed, as when modern nations
compete and often combine to engage in warfare as a single unit. Such expansions
can result in extensions of positive sociality and the potential for ultimate global
harmony.
Note regarding positive sociality: The somewhat indefinite but frequently used
concept of “altruism” implies that a gift-giver is prepared to contribute to others
without reciprocation. But the shakiness and early termination of one-way flows of
benefits make little sense, except to “free riders.” Sense takes hold when gifts begin
to be reciprocated—when altruism is converted to reciprocity. Reciprocating
positive interactions tend to become the rule in successful social life. Perhaps we
can simplify and clarify by considering somewhat different terminologies. Thus,
net-cost altruism straightforwardly offers little or no likelihood of return benefits,
as its name acknowledges; it is the definite version of a solid concept, but not a
useful vehicle in the organization of sociality, and not likely to represent expand-
ing and cooperative sociality. Social investment, as a replacement for the ambigu-
ous “altruism” (used frequently in quotes because of its vagueness), is obviously
prepared, and is expected to pass benefits to needy or willing reciprocators. Net
cost altruism turns into social investment when either reciprocators or incidental
394 { Human Social Evolution

observers of social investment decide to give or return benefits to social investors.

Reciprocating partners, providing return beneficence to social investors, create
return flows of benefits to apparent or obvious social investors. Social invest-
ments, in responses with return beneficence, can support extensive, or even vast,
networks of continuing and ever-expanding positive sociality that may have the
wherewithal to generate and expand pockets of cooperativeness and unification as
prospects building toward global harmony. Mutualism is the term applied when
individuals gain from uniting (or cooperating), or when members of different spe-
cies do so, because in each of such cases the combined benefits of the involved
individuals can contribute, without risk, to partners that produce reliably reward-
ing, useful evolved benefits.

MYSTERIES OF THE MIND, AND THE MUTING OF CONSCIOUSNESS

When people do spend most or all of their time peacefully, we are likely to ask two
questions: First, why is it that wars and other serious conflicts seem always to exist,
somewhere along the horizon, reminding us that even our most congenial friends
may either succeed in war or disappear prematurely as a result of participation in
war? Second, how and why do people often, or virtually all of the time, forget or
ignore entirely the sometimes horrendous events that loom almost permanently
somewhere along those personal horizons?
For a moment we can pause and remember that we humans have evolved in
the same ways that other organisms have evolved. However, unlike the millions
of individuals in species that maintain themselves despite diseases and predation,
along with high rates of accidental or incidental deaths across the lifetimes of indi-
viduals, large numbers of humans are all too likely to die from deliberate attacks
at the hands of members of their own species. Why is it that we are so adept at
forgetting or ignoring the trials, terrors, and truths that affect our fellow humans,
and ourselves?
Surely, not everyone is prepared to argue that natural selection can reduce
sensitivity or recall specific knowledge of previous unpleasant or deadly activities
affecting ourselves or others. Most likely, we think that we simply forget. Or such
activities may be removed from our consciousness because they are unpleasant, or
because we become convinced that those events were not nearly as traumatic as it
seemed when they were happening. But consciousness muted by natural selection
is not likely to be a simple error, and it can be a much more significant change than
is easy to comprehend.
Not long ago Dr. Billy E. Frye, former Provost of the University of Michigan
and Chancellor of Emory University, wrote to me as follows (I have paraphrased
slightly in some places):

A recent note from an elderly friend reminded me that many people, even
well educated people whom I respect very much and who have no difficulty
 Evolution and Religion } 395

accepting the idea of human evolution (vs. miraculous creation), still cling to
some sort of metaphysical idea about the mystery of humans, or the mystery of
life. On several occasions this question has come out in a context that makes
it clear that at some level people resent, or regard as futile and undesirable,
attempts to explain human nature in evolutionary terms. They seem to hold on
to the notion that there is something spiritual about us that cannot and should
not be “explained away” by evolutionary considerations. In at least some of
these instances, perhaps all, it is clear that people like and are wedded to the
idea of grand mysteries that will never be resolved—to the notion that there are
things about us that we will never understand.
Two questions occur to me: First, why do people like the mystery of the
unknown? In this case they clearly do not regard it simply as an exciting chal-
lenge. Is it because we can cling to the feeling that something is unchanging
and will always be as it is now? If that is so, it strikes me that this is religion in
its most basic essence. It seems to me that mystery in this sense may be a way
of preserving as untouchable some sentiments about a spiritual realm without
ever naming it as such, without becoming literal about religious belief in the
way that, say, biblical fundamentalists do. I have the impression that some
of us want our universe ultimately to be infinite and unchanging, and in a
way the notion of the grand, unsolvable (perhaps spiritual?) mystery puts a
finite boundary around the universe of our imaginations and our intellectual
probings.
Second, is it possible that part of the resistance to acceptance of evolution by
many social scientists and humanists originates in this kind of desire for mys-
tery—for unsolvable, unapproachable mystery? In support of this notion I will
only observe that at least some of those who have resisted the recent emergence
of evolutionary explanations have exhibited overt resentment, and even hostil-
ity and anger, toward both these ideas and the people who expound them, and
sometimes have openly scoffed at the very idea of trying to explain the “inex-
plicable mystery” of humans. It is in this sense that I ask, why do we cling to
mystery with so much passion? (Dr. Billy E. Frye, personal communication)

My first response to Professor Frye’s relevant and provocative comments is that

everyone may, in fact, have some realization, expectation, desire, and capacity for
mystery. Perhaps that is part of the feeling expressed by a minister who declared
that he was not interested in a concept but the real thing—the real God. Perhaps he
meant, at least in part, “a persisting and unchanging mystery,” perhaps the concept
of God that has been accepted and formed mentally as matching the understand-
ing of the minister’s own life, and seeming to hover continually over all of human-
ity. In my view it is part of the argument for acceptance of diverse concepts of God
that our feelings about the mysteries surrounding religion—and our uses of such
concepts as God, Eternity, Heaven, Hell, and Purgatory—deserve the attention of
anyone interested in the topics of this essay.
396 { Human Social Evolution

For me the next question is whether there is a relationship between the mys-
teries of religion and its various contexts, and the everyday activities, thoughts,
and wonderings associated with the life activities of humans, in particular their
kin interactions and other kinds of social affiliations. I think there is such a rela-
tionship, and I also think it is not entirely a consciously accepted or analyzed
phenomenon—hence, perhaps, in that sense it may remain a mystery that can
potentially serve the combined interests of all people via a universal or global
version of God—or via prominent and influential individuals or groups that
have incorporated such universal or global mysteries under the rubric of a
supernatural God.
We are strange organisms, both immensely social and intensely confrontational
within our own species—indeed, within our own social groups. It is as if humans
have evolved to maximize two phenotypes, in the way that thousands of organ-
isms have been able to emerge as either of two (or more!) different phenotypes,
sufficiently distinctive that the different forms often have been regarded as differ-
ent species. Humans, too, have evolved so as to be knotted up in the differences
and significance of dualities—not merely war and peace, but such as conscious
and unconscious, honest and dishonest, other-deception and self-deception, and
with kin-group and friend-helping of our “in” or “we” group, as contrasted with
the competitive and adversarial “they” parts of other groups—we-they or amity-
enmity axes. Biologists have been able to explain the dualities and otherwise dif-
ferent phenotypes in terms of environmental differences, but they have not yet
clearly and completely explained how humans can change themselves more or less
suddenly from gentle, helpful, congenial people into extreme military warriors.
Part of the reason for thinking about mysteries derives from the fact that the
kin circle or any social group is itself likely to be somewhat mysterious, perhaps
because it is a social unit composed of numerous genetically or socially connected
individuals. Trying to cause any such social group to function as a unit can involve
many kinds of agreements and disagreements, influenced by overlapping social or
kin relations, and reflecting as well the hierarchically arranged organizations and
other elaborations of religious demands.
Part of the mystery of such social groups exists because, other things being
equal, humans are evolved to treat their kin or their associates according to the
extent of their social history or their overlap in genes identical by immediate
descent; but the people involved may or may not be entirely aware of the relation-
ship. Considering kin, we can know the order by which familiar relatives are in
fact related to us; and we can be conscious that the more generational links that
descend between us, the more distant is the genetic relationship. In this sense, and
in the sense that a kin group consists of genetic relatives, the mystery is not so
deep. But, to repeat, a good deal of what makes a kin or other social group func-
tion surely is not consciously grasped by all of its members.
When one considers these topics, it becomes obvious that we humans are always
thriving on mystery—in part at least mysteries within ourselves that we typically
 Evolution and Religion } 397

do not wish to reveal completely. In some sense those mysteries relate back to that
“nasty hoard” in the “secret cellar” that Stanley Elkin (1993) mentioned when com-
menting on the incompleteness of all autobiographies, and what we don’t want
to reveal (cf. Alexander 2010). And we are back to the fact that we do not always
know what to do or why we (or religious leaders) do certain things. We don’t know
consciously how much or what to reveal to others, not even to close kin, and not
even if we sense unconsciously what maximizes the quantification that was never
known to us before the recent rise of the sciences of biology and evolution—and
that quantification is a consistency in the behavior of genes, termed the maximiz-
ing of inclusive fitness. There are many situations, indeed, in which the biological
principles of organic evolution are the only way to explain how organisms, includ-
ing the human organism, can be understood.
People may want the concept of God to be true, at least partly so, because God
is a concept that has come to represent the holder of secrets about ourselves—
actually, is typically considered the keeper of the secrets—the source of confiden-
tiality, the reasons for almost every aspect of accepted knowledge, and the means
of making everything right for us when the time comes. I have used “secrets” here
in a very broad way, but the word “mystery” is probably better. Take that concept
away, and we may believe we have somehow diminished the quality of existence.
Kin groups can have similar effects (leave aside, for now, the rest of our lifetime
associates). Examples can be a slight or great mystery, a “storehouse” of knowledge
that can be used either against or for nearly anyone in the group, depending on cir-
cumstances and the interactions of members of the kin group. Perhaps it is merely
that we are acutely aware of our continuing inability to enter, absorb, and fully
understand the workings of the minds of our individual and congenial compan-
ions, not to mention hordes of acquaintances, passersby, and complete strangers.
After all, human individuals function constantly, necessarily mysteriously, and in
domineering and moral elaborations within the continuing performances of their
own uniquely extensive, and always to some extent, private desires and intellects;
their extensive, complicated, and long-lasting memories surely function unlike the
members of all other species.
I think there is a way to understand why we don’t want ourselves to be entirely
non-mysterious, even for the people to whom we are closest, and certainly with
respect to everyone else. Our hesitance can be partly as if, should we reveal our-
selves to anyone (or everyone) completely, we would also be “completely” vulner-
able—for example, to reputational derogation, whether justifiable or not (we are
good at manufacturing the unjustifiable kind!); and scorn and the opportunity for
all of our associates and potential enemies to threaten our ruin by telling our ene-
mies about everything negative or demeaning about us that they can muster, along
routes that affect us in the worst possible ways. Perhaps some people are convinced
that science will “out” all of their personal privacies, and all of the special (good
and bad) things they think about themselves. It becomes a global proposition to
protect ourselves from that kind of competitiveness and one-upmanship, although
398 { Human Social Evolution

protection is also available because of revealed knowledge of demeaning actions

susceptible to open disclosures.
I think people see as threatening—direly threatening—any possibility of com-
plete unraveling of our individual complexities, such as many people may think
will happen if scientists keep probing the nature of humans. My view, however, is
that the probing can never be completed, and one reason is that the probing—the
continuing exploration within the human mind—will inevitably extend, with hope,
and beneficially, the array of cloistered, sequestered, changing mental strategies and
subterfuges. This is a pattern that returns us to the realization that we have evolved
to compete—literally to outcompete others attempting to outcompete ourselves.
It may be slightly disheartening that individuals of any species have evolved
to control or outdo other individuals, despite group cooperation, and in humans,
despite denials. After all, the intentions and consequences deriving from the evolu-
tionary selection that continually influences us all as individuals are, in some way,
whether clever or clumsy, evolved to outcompete any and every other associated indi-
vidual that does not provide return beneficence satisfying the silent and potentially
negative or critical thoughts of affiliative but also secretive individuals. This is a basic
relationship of all individual humans, whether or not it is recognized or accepted
widely, and despite the parallelism in the congeniality of profitable group-living.
It is a relationship that may explain the universality of both human mysteries in
general, and the consequences of utilization of such mysteries by those who may
seek reasons for promoting group behaviors that can develop hierarchically domi-
neering and extravagant ceremonies. Included are the almost universal establish-
ments of lavish and ostentatious houses of worship, generated and operated by
individuals behaving as morally superior leaders representing themselves as God’s
close aides and collaborators—and with little doubt considering themselves to be
special individuals interpreting messages transmitted directly and frequently from
a supernatural God.
I do not wish that the aspects of religion just described, or religion in gen-
eral, should wane or disappear. Instead I wish that church officials and members
alike can begin to regard themselves and their particular religions and activities as
potentially students of social and universal success, as results of science as well as
religions, and including concepts of a universal God that serves a universality of
social success, and does not fragment the world of religion into prideful factions,
sometimes bitterly disagreeing and war-like.
In any case, it seems clear that humans demonstrate multiple features that are
collectively relevant to the questions of religion: mystery, human consciousness
and its changes, and human competition and cooperation. Natural selection has
caused human individuals not only to work together in appropriate circumstances,
but as well to compete with other individuals, and to compete group-against-
group. Competition among humans has surely caused natural selection to con-
tinually expand and magnify human mental activity. Unlike most other species,
and in some ways like all other species, humans have become capable of unique,
 Evolution and Religion } 399

complex, and continual mental activities. Some of such mental understanding and
activities of humans are likely to be withheld from other humans, withholdings
that maintain and influence much of the information in the mental activity of
humans. This combination of hidden human traits will always create and maintain
mystery. As long as the brains of humans continue to expand their views, and
their understanding of themselves and their associates and competitors, no one
will escape the presence and continuance of mystery—the mystery of personally
functioning human minds, working both singly and collectively in their own local
environments.
It therefore seems entirely possible that mysteries which puzzle us, and con-
front us continually, are results of (1) the competitiveness of everyday ordinary
individual humans, and (2) congenial groups of cooperative humans and conge-
nial groups of competitive humans. Even more fascinating is the probability that
the current mysteries of humanity were absorbed and became—or expanded
into—the mysteries that have generated and continued to elaborate the basis of
religion and the concept of God.
It should not be surprising that people, as individuals or in groups, have been
ready to accept special individuals with skills to claim knowing of attractive and
unworldly mysteries, presumably from their own experiences and backgrounds;
special individuals that use their special qualities to connect with people that
in some circumstances wish to control while making others into subordinate
beings, thereby generating organized systems of domination, explicitly glorify-
ing differently special individuals or groups that can be made unusually useful.
Can we deny that virtually the entire program of religion could have originated
from the value of its organization of the various groups that have spread across
the planet? How might we discover whether such effects have served the ele-
vated and impressive ceremonies that have persisted and spread since, explic-
itly because they were attracted to the mysteries that have been carried always
within the souls and consciences of humans? Is it not possible that these argu-
ments, these not merely particular but as well universal human mysteries, may
be constantly reflecting a mixed combination of secular and formally religious
backgrounds that together could become parallel services across the entire pop-
ulation of the world?
***
Humans collect within their brains all manners of learning that they hold on
to indefinitely, without necessarily thinking about them—items of knowledge
that people can bring back to their consciousness, but do not always do so.
Examples are foresight, memory, cognition, reflecting, itemizing, organizing,
storing, combining, interpreting, scenario-building, and many additional intel-
lectual capabilities that can remain functional across impressive portions of the
durations of our active lives.

***
400 { Human Social Evolution

WARS, GENOCIDES, AND MURDERS

The Most Important Failures of Humanity, and What Can Be Done about Them
As readers look through this essay, I would wish to be able to ask a series of ques-
tions about the topic of this section. Specifically, I would like readers to (1) ask
themselves to estimate the numbers of population deaths in various different situ-
ations known to involve wars or genocides (for examples, see below); and (2) con-
tinue to ask other people the same question. See for yourselves the accuracy, or
absence of accuracy, from those situations, and consider reflecting on the topic of
muted consciousness (see also, Pinker 2011).
***
Humans are collectively, uniquely, and by far the most ferocious, hyper-com-
petitive, hyper-patriotic, war-mongering, genocidal, and murderous species
on earth. Unlike all other species, we humans have become (or maintained
ourselves as) our own worst enemies. We have made it so by dramatically
diminishing the significance of other-species enemies and increasing the num-
bers, crowding, competitiveness, and conflicts of members of the human spe-
cies. As an example of one such consequence, one study of deaths from wars
and genocides alone, during the twentieth century, has yielded a maximum
figure of 150–160 million such deaths, averaging approximately 4,000 deaths
per day—counting every day of every year across those 100 successive years
(Scaruffi 2006; see also Goldhagen 2009; Pinker 2011). During the United
States’ Civil War, a war with far fewer citizens, war deaths were calculated at
618,222 (Encyclopedia Americana).

***
In the Ann Arbor News of March 29, 2012, The United Nations has estimated
that more than 9,000 individuals have been killed in recent continuing dis-
agreements between the Syrian dictatorship and its citizens. The UN has since
increased the death count in Syria’s civil war to at least 60,000 people.

***
On the morning that I wrote this paragraph, 74 people were reported to have
died in Egypt during a relatively brief turmoil involving primarily a single con-
troversial soccer game.
***
The city of Detroit, Michigan, reported on ABC television that, during the past
year, 344 people were murdered—only 21 fewer than one person every day
across the entire year.

***
 Evolution and Religion } 401

Kill a man, and you are an assassin. Kill millions of men, and you are a con-
querer. Kill everyone, and you are a god.
—beilby porteus (1731–1809) Bishop of London
***
A hydrogen bomb is an example of mankind’s enormous capacity for friendly
cooperation. Its construction requires an intricate network of human teams,
all working with single-minded devotion toward a common goal. Let us pause
and savor the glow of self-congratulation we deserve for belonging to such an
intelligent and sociable species.
—robert S. bigelow, 1969: The Dawn Warriors
***
Movies, operas, fictional and nonfictional stories, books, and other accounts
and documents demonstrate the hyper-competitiveness and hyper-patriotism
that reflect the duality of geniality and ferocity, of loving and hating, which
seem to be maintained, and in certain ways are not only considered accept-
able, but are relished, at least sometimes, in the minds of most humans. Over
and above wars, all across the United States, the morning news lists small and
large numbers of recent deaths by murders of single individuals, families, or
other small numbers of people, accomplished with definite purpose, despite the
strange fact that most publicly revealed felony murderers have to realize, prior
to their decision to kill, that they are predictably doomed to lifelong incarcera-
tion—or else lose their awareness of their oncoming mistake(s).
***
How did this situation come about? What are the continuing reasons for it?
How can it continue to be prevalent? Why do so many people tune in every day
to trace ongoing, potential, and fictional(!) wars, and to hear about the details of
morning and evening single or group murders, and attempts at murder? Why do
humans multiply and sustain heinous and despicable behaviors, emphasizing and
detailing endless varieties of films, fictional programs, and other performances
in which multiple murders are made to appear as horrific and chilling as pos-
sible, using words like slaughter, assassination, lynching, decapitation, throat
cutting, strangling, suffocation, drowning, bludgeoning, poisoning, disembow-
elment, serial killings, and many other incredibly diverse and sickening ways to
vilify, nauseate, terrify, and destroy members of our own species? Why do real
and imaginary happenings appeal so completely as to make even fictitious horror
publications, movies, and shows simultaneously seem both devastating and thrill-
ing? On what basis can we imagine movement toward a global harmony when so
much of our interest is linked so frequently to such almost constantly negative, yet
thrilling experiences?
402 { Human Social Evolution

Consider the great number of old-time western films, or “cowboy movies,” in which
nearly every actor is likely to carry ostentatiously at least two guns, and maybe knives
as well, and in which small and large numbers of seemingly unfortunate actors and
actresses are taught to pretend that they are being slaughtered in the most horren-
dous fashions. Why are virtually all such performances so persistent, and so incredibly
and abundantly popular? Is it simply because people have acquired deadly weapons,
and have learned with practice, and in the absence of sufficient legal control? Or is it
that they believe they can slaughter those who are apparently or potentially competi-
tive, unfriendly, or vulnerable? What has caused the success that seems to represent
repulsive, disgusting, and appalling aspects of human nature? Why do we apply such
extraordinary varieties of different terms to modes of deliberate killings? Why do such
attitudes continue to persist, and to be regarded as honorable or laudable? How do we
also manage to erase temporarily, and so easily and quickly, the horrendous examples
laid out before us in the news media and in nearly all forms of literature and diverse
performances? Is it merely that the expansion of deadly weapons has magnified the
likelihood of besting individuals and groups in particular situations to motivate use
of every instrument and method to outdo other competitive individuals and groups?
I suggest that this situation can be partly understood by considering together
several major aspects of human performance linked to events or circumstances
that, evidently across most or all of human history, have generated combina-
tions of human traits and tendencies that bring together diverse components of
human nature, and produce the current and now essentially universal and deplor-
able human situations. Continual expansion of increasingly devastating weapons
provides reasons for extending methods and plans for fighting individuals and
groups, today including huge and sometimes multiple nations coming together to
create incredible havoc in war. Differences in power and motivation from chang-
ing weaponry and strategies can continually reinforce tendencies to bully, attack,
batter, kidnap, rape, eject, banish, and kill potential or actual competitors. Is it
really an exaggeration to say that all we have to do in group-against group con-
frontations is to change to our rules and proceed?
Aside from bonding of male-female interactions, parent-offspring and other
kin relations, and the clustering together of non-relatives in the interest of saving
themselves via the strength of their group against other hostile groups, the mem-
bers of all species seem to have evolved to do their best to outcompete all others
in one way or another within their vicinity. It would appear that the members of
no species anywhere can even remotely match the “grandly” intelligent members
of the human species with respect to continually revising and rendering weapons
and strategies increasingly more devastating, and magnifying temptations to kill,
bully, or drive away other humans.

Team Competitions in Sports

If humans have become their own principal hostile force of nature, we might eas-
ily understand how humans have also become the only species known to play
 Evolution and Religion } 403

competitively, group against group, in team sports—in groups that win or lose
as groups (Alexander 1967–2011). Team sports are forms of play. Most biologists
regard play as having evolved as practice—practice for something other than
play—instead, for the “real thing,” which in this case can only be competition and
conflict, perhaps—ultimately—direct or indirect contributions to warfare between
human groups.
It is not easy to deny that the raging excitement of such games, including, for
example, deliberate distractions by fans (enthusiasts) with loud noises and raucous
actions, for example, rapidly flapping devices that create a virtual “field” of noise
and confusion in front of a player who is attempting “free”(!) throws. Such devices
are designed to confuse and thwart players on the other team.
Teams competing in sports are exhorted to think only of the team, not of
themselves as individuals. That is precisely what takes place in the military, in
which individuals are dramatically, necessarily, and cleverly (especially when war
is imminent or current) subordinated to the service of their functional units and
trained to perform as members of closely-knit, single-purpose groups. They are
individuals prepared to give their lives to save the group, all of it or part of it. In
some sport arenas, the intensity of team sports results in more than 100,000 on-
site spectators.
We can consider whether it is possible for widespread and intense team sports
to remain true to their apparent original purpose. One question is how to gener-
ate such considerations in the interest of promoting social harmony. Games and
other activities, including both individual and team sports, may have replaced
and reduced the incidence of serious, intense, and negative forms of competition.
But hateful conflict, too-frequent killings, and other negative encounters—the lat-
ter curiously more often by over-zealous fans than by team members, and with
equally avid appetites for increasingly horrendous cinema, radio, and literature—
have shown little evidence of receding or disappearing from competitive team
sports, or from shocking or gruesome theater in all of its variations.
It might be enlightening to rank the frequencies of incidental or accidental inju-
ries to players and fans in the different sports of basketball, football, hockey, and
soccer, and compare them with the frequency and severity of injuries from physi-
cal altercations to players and fans. A significant example is the recent report of
instructions, or tutelage, by coaches, about pre-arranged attractive cash rewards,
offered to professional football players who are then expected deliberately to cause
disabling injuries to opponents.
Surely, we all hope and expect that the positive excitement and enjoyment of team
sports will continue, and thrive, and that serious team and spectator tensions will
continue to identify methods and reasons to soften and adjust their actions without
eliminating the excitement and enjoyment of competition. There are reasons for
team sports to minimize the potential for generating extreme actions and attitudes
that expand and direct the shadows of serious conflict and warfare. It seems pos-
sible—and of great significance—that, with care and thoughtfulness, large increases
404 { Human Social Evolution

in sporting competitions, on international scales, can become extraordinarily valu-

able contributions to continuations of positive cooperative and competitive sports,
and to reduction or elimination of seriously negative consequences.

Humans Have Created Their Own Principal Hostile Forces of Nature

Unlike members of other species, humans living in groups are extraordinarily— prob-
ably in some ways uniquely—competitive within their own species. Wars, genocides,
murder, bullying, injustices, dishonesty, deceit, fraud—all such results of hyper-com-
petitive, hyper-patriotic behavior—are “hyper-prevalent” in humans. Again, we are
reminded that natural selection tends to maximize reproduction, and that we accom-
plish this by as nearly as possible out-performing everyone but ourselves.
Following, in some respects, Sir Arthur Keith (1949) and Robert S. Bigelow
(1969), I have suggested that modern humans have, for better or for worse, consid-
ered other humans, especially in groups, to be their most important hostile forces
of nature. Part of my argument began with the possibility that only this feature can
explain why the expensive human brain has evolved—or persistently increased
in size and complexity—so far beyond the brain sizes of its closest primate rela-
tives (cf. Alexander 1967, 1968, 1979, 1987, 1990, 2008). If this argument is correct,
then we can see another way that humans living in groups can be behaving self-
ishly when they save or help members of their own groups but not those in other
groups. When we realize the rates at which people have been killed in wars and
genocides, even during the 20th century alone, the emergence of larger human
groups and more deadly and catastrophic weapons may become more devastat-
ing than we might have anticipated (e.g., Ember and Ember 1990, Scaruffi 2006,
Goldhagen 2009, Pinker 2011). If we turn away and simply accept the manner in
which differential reproduction functions—and if selflessness, cooperativeness,
and social reciprocity do not function so as to build social harmony—we will be
yielding to the relentless slow changes of natural selection, and failing in the effort
to enhance the possibility of roles for effective social investment and return benefi-
cence in our societies.
Balance-of-power races between different groups of the same species may be
uniquely important in human evolution (Alexander 1979, 1987, 1990, 1993, 2005).
The particular forms and sizes of group-living to which humans have been driven
by this unusual situation have caused dramatic changes in entire collections of
related traits, suggesting that whatever caused the human kind of group-living
were dire and continuing threats. The organ most dramatically affected is likely
the human brain, because of the usefulness of social cleverness and expertise in
interactions among individuals of the same species.

SCIENCE AND RELIGION

In my view, it is not necessary, or useful, to disparage the concept of faith. All of us
conduct our lives with a large complement of faith. There is no effective alternative
 Evolution and Religion } 405

because we simply do not have the means to learn for ourselves about everything
we would like to understand. The difficulty with the concept of faith is that, par-
ticularly in religious contexts, most expressions of it seem to require absoluteness.
Thus, by claiming a basis in eternal verity deriving from an unchangeable super-
natural source, faith sometimes takes forms that call for permanent incontrovert-
ibility. This assumption is closely related to permanent assumptions of value in the
moral rules of humanity. It inevitably becomes adversarial to all of the ways—all
of the formal and informal procedures—according to which we learn by exploring
the nature of the physical and living universe. Science, whether formal or infor-
mal, necessarily changes continually as knowledge accumulates, while moral rules
tend to be enforced and maintained, therefore tend to be lasting and unchang-
ing, sometimes by declaration, whether right or wrong. This, and the difference
between morality and reality, is a source of conflicts between a science of discovery
and a faith supporting agents of supposed unchangeable immortality.
Scientific procedures are effective because they eschew attitudes of “blind faith”
in favor of testing repeatedly—and continuing testing—until results are obtained
that can be verified by repetition. But we do this not merely in formal scientific
investigations but also in all of our ordinary activities. In everyday life even the
most devout persons employ “scientific method” almost continually. When prob-
lems are encountered, we generate guesses, or ideas, about possible answers, then
do whatever is necessary to see if the idea is correct. If it is demonstrated to be in
error, a new idea has to be generated and tested. If we are preparing a meal, we
may taste the results repeatedly so as to try to improve what is cooking, testing
and retesting to get the desired results. Exactly the same procedure is used in try-
ing to find out why our automobile has stopped running, or why a child is brought
to a physician to analyze and diminish or remove a serious ailment. As soon as
an idea passes all the tests, one by one, the person doing the testing can proceed,
using the new knowledge. That is precisely the kind of procedure that is used by
scientists at work. Typically, this simply means generating the next hypothesis,
or guess—as suggested by the Nobel Prize–winning physicist, Richard Feynman
(see Sykes 1994)—and continuing, or else starting the whole testing process again.
The more complicated the problem, the more complicated the process of gener-
ating worthwhile possibilities and testing them. Willingness to seek alternative
explanations, and to revise our understanding of every investigatory process are
the hallmarks of success in finding the truth—of discovering how to “get things
straight.” As already suggested, insistence that faith has to be absolute and perma-
nently unchanging because it derives from supernatural forces—and that science
is therefore the enemy of faith (and in this sense, the enemy of rigid and unchang-
ing authority—derived morality)—is probably the most serious conflict between
religious and non-religious practices (see the extensive and provocative discus-
sions by Dennett 2006, on religion as a natural phenomenon). This set of conflicts
is likely to increase as scientific knowledge expands, while religious faith may risk
clinging to long-continued but perhaps no longer acceptable claims.
406 { Human Social Evolution

THE MEANING OF LIFE

Acceptance of the arguments made earlier enables us to repeat two related propo-
sitions about the effort to characterize God and the mysteries of humanity: (1)
the concept of God as an outcome or consequence of human evolution, derived
from the flow of human intelligence; and (2) the meaning (or purpose) of life can
be to serve, and probably always has served, as what may be termed a universally
acceptable metaphorical spirit, by many thought of as God, and generated via the
mystery that is the “hoard” of more or less unstated and unrevealed knowledge
that persists, each with its own uniqueness, within every human being’s special
mind and imagination. The first-numbered statement above has been character-
ized in such a way as to clarify what is meant. The second statement, however,
deserves further discussion.
When the concept of meaning is explored, as by returning to the dictionary
(repeatedly!), one finds it treated as mainly synonymous with purpose, aim, and
intent. In other words, meaning is virtually always treated as anthropomorphic—
as requiring motivation of the sort that humans exhibit when they set out con-
sciously to achieve something, projecting alternative behaviors into the imagined
future in a testing way. If one asks “What is the meaning of life?” the answer will
be quite different if “life” is meant to refer to all of human life, as opposed to the
individual life of a human being. We cannot easily answer the question of mean-
ing for non-human forms of life or nonliving parts of the universe unless or until
we accept the idea that the same concept that “created” humanity (using either of
the common meanings of humanity) also created the physical universe and non-
human life. Otherwise nothing could give meaning to non-living objects or non-
human life, other than evolved function per se, to all indications never conscious
or self-perceived except in ourselves. This is so because, even if we can work out
evolved function, we cannot easily translate into intent or purpose the ways in
which nonhuman forms of life, especially those apparently lacking anything even
remotely resembling consciousness, use environmental stimuli to respond appro-
priately to events as they arise. As a concept associated with conscious thinking in
humans, meaning is possibly without any counterpart among non-human living
forms. Only human life can confidently be said to have conscious purpose—or at
least very much of it.
Purpose could be ascribed to a human life from two backgrounds. First, I might
ask myself what is the meaning of my personal life. In some sense I could make
it anything I please. But I suggest we would all agree this would be a difficult atti-
tude to assume and maintain. I think we have to assume that this difficulty is a
consequence of the tendencies and capacities allotted to us by our evolutionary
history. Thus, it is likely that difficulty would arise because we are not evolved
to have such a motivation, or to give such an intent or purpose to our lives. We
may not be evolved to answer the question of personal meaning at all, at least in
any general or long-term sense—even if we seek it plaintively sometimes. On the
 Evolution and Religion } 407

other hand many of us have been exhorted at one time or another to give our lives
to God—to consider our lives as service to God. But it is difficult to do this—to
imagine any meaning for life—unless we accept that an anthropomorphic spirit
or attitude formed our lives, or governs them—said differently, created a universal
phenomenon, embodying intent among ourselves. This requirement can be met,
or accepted and used, not only potentially by a traditional, personified, and in our
best thinking, universal God; but also by the spirit or thought process generated
out of the human moral capacity, historically residing in the collective minds of the
kin group or minimal defensive unit, and expressed from that collection of minds.
Second, and following arguments given earlier, the purpose or meaning of
human life as a more general proposition becomes a question. Purpose is some-
thing that individuals have so that, as said, we can think about our own lives as
having whatever purpose we choose to give to ourselves, whatever purpose we can
mount under the a priori thrust given to our lives by our personal experiences and
by the evolutionary process (a priori in the sense of pre-dating or using our per-
sonal consciousness to inject purpose or intent). We can also consider the purpose
of any outcomes of confluences of interest with other individuals, or group inter-
ests, to which we subscribe or accede. Nathan Hale must have been an extreme
example when he supposedly said: “I regret that I have but one life to give for my
country.”
So life per se (or in general) probably never had anything legitimately termed
a conscious purpose until we generated something that could give such purpose
to it. As already noted, that “something” was probably generated as an anthropo-
morphic cause for life—a Creator, designated or named as “God.” It is a spirit that
gives purpose to life—for many or most people now, but potentially, and most
effectively, for all people, as a universal concept (See also, Dennett 2006).
We can wonder if portions of the arguments made here were sufficiently avail-
able to the psyches of an ample number of humans across the appropriate portions
of history for them to realize consciously that they might have to come up with
an anthropomorphic God if they wanted to assure themselves (or others—e.g.,
potential Nathan Hales) that life in general has purpose—in the same sense as
human purpose. That is, there had to be purpose from some source other than the
“mereness” of ourselves as individuals or the slightly larger mereness of our local
groups—the competitive (defensive, aggressive, warring) and cooperative units.
Further testing of the approach presented here lies partly in persistent efforts
over long times to apply the proposed concept in every life situation: (1) to ask in
every instance in which God is mentioned or invoked how apt in that instance
is the concept of a universal spirit of beneficence; and (2) to see if the concept of
such a universal spirit ever becomes impossible, or how often it is more awkward
or more reasonable than its alternatives: whether it appears to explain each and
every situation, excepting those which turn out upon closer examination to have
been based on factual error.
408 { Human Social Evolution

Understanding of the group morality concept of God, and its effective use,
also requires that we seek a better understanding of the moral capacity—or its
expression as conscience or as willingness to invest socially (and even to hone such
willingness by practice in solitary or in anonymity)—that surely characterizes all
humans everywhere. Assuming that as individuals we start out socially naive, how
do we change under different social stimuli so as to mature what is likely to be
regarded as a “normal” concept and effective practice of morality? How can we
accomplish this increased understanding so as to promote a concept of God (or a
set of such concepts) that can be truly universal? How can we move toward world
peace rather than, ironically, primarily enlarging the sizes and frightening capa-
bilities of a smaller number of more horrifically willing and aggressive nations?
We need to reflect on how difficult it might be to deny that this is the most we
wish to understand about what God and democracy-loving folks have been able to
accomplish, while continuing to lack significant prospects of universal peace from
the directions taken so far.
I have not discussed the deterioration that causes the invariable termination
of the human lifetime. It is well known from biological science that this deterio-
ration results from complex changes in the survivability of the genes and cells
of organisms under negative environmental influences across the later parts of
life, and that reproductive potential loses its effectiveness as the organism ages (cf.
Williams and Williams 1957; Williams 1966; Alexander 1987; and many others).
It would seem that being aware of the sad certainty of the end of life may have
accounted for the ancient religious belief that death could be turned into a mere
transition to a supernatural place called heaven. As biological studies continue on
an ever-broadening scale, and are increasingly well understood among the com-
plexities of the evolutionary process, the connections and relationships between
the organization of life’s recently analyzable processes and the assumptions of reli-
gion, generated centuries ago, will certainly continue to modify our views of life.

MORALITY AND THE EFFORT TO PROMOTE UNIVERSALITY OF GOD

The evolutionary approach to human behavior continues to have serious problems.
As suggested earlier, the most obvious one is that evolution is accepted by only a
minuscule proportion of the world’s population. Even within that minuscule pro-
portion, too many academicians and intelligentsia tend to wall evolutionists off
as if they were malignant tumors. This happens partly because only a minority of
thoughtful people are extensively educated in biology, and this in turn is partly
because the interaction of heredity and development (the generation of the indi-
vidual) is still poorly understood. Also contributory is the convoluted nature of
human efforts to self-understand, not only because we must use the properties we
wish to understand to carry out the analysis, but as well the nature of the biological
history that few wish to contemplate. It is not easy for anyone to believe, from his
or her thoughts about personal motivation and that of other humans, that humans
 Evolution and Religion } 409

are designed by natural selection to seek their own interests, let alone to maxi-
mize their own genetic reproduction. Natural selection appears to have designed
human motivation in social matters in such fashion as to cause its understanding
to be resisted powerfully.
We lose in analyzing such problems, if we restrict ourselves to discussing only
the brighter side of human nature or pretend that the topic is cooperation, and
not competition as well. Some moral philosophers and other academicians seem
to travel mainly in pleasant worlds, as if with little opaque clouds that tend to
admit only the delightful aspects of human intentionality (or their shadows) float-
ing above their heads as they move along the sidewalks of Urbania between their
offices and their homes. But the misery in the world is not all there because of
pathologies easy to understand or proximate causes easy to remedy. Nor is it all
owing to those “other” kinds of people whose motivations (unlike our own, of
course!) are sometimes pernicious and self-serving. Moreover, technology and
civilization (weapons and war) have created circumstances in which virtually all
human striving, designed as it is to better the current quality of life, nevertheless
continues to threaten increasingly the future of humans, even that of our planet
and life itself.
Analysts of morality must retreat from their subject far enough to examine the
reasons for its convolution. We will gain from understanding that the kindness,
beneficence, and good fellowship that occurs or remains only locally tends to be
selfish, and we must also understand why the idea is repugnant and what to do
about that. To solve the problems that human evolutionists have glimpsed so far,
we will gain from enlisting a far greater proportion of the world’s thinkers. If, as
knowledgeable people increasingly suggest, massive beneficence by our genera-
tions will be required to ensure the survival of later generations, then unless we
don’t care we have to know how to reverse the relevant aspects of the striving we
have evolved to accomplish. We have to know how to use the fact that no part of
biological theory has ever legitimately implied that humans cannot employ their
evolution-given traits to set and accomplish goals that are entirely incidental—
even contrary—to negative aspects of their history of natural selection. I would
suggest that these things will happen only when evolution-minded people have
overcome resistance to evolutionary analysis of behavior by explaining, much bet-
ter than has been accomplished so far, the nature of human motivation and the
reasons for its partial concealment and seeming withdrawal.
The capacity to generate an effective moral sense is surely a criterion for all-
privileges membership in our species. Suppose that the concept of God does
indeed arise out of cooperation and good will, and our reciprocating confidence
in the existence of the people involved; and suppose that in the mind of every
individual the concept actually stands for that collective of cooperation and good
will (whether entirely consciously or not). This would mean that beneficence
and charity derive from our sensing of the social power, will, and value of, not
an extrinsic human-like being, but the mind (and minds) of the collective itself.
410 { Human Social Evolution

Surely, then, it is a reasonable speculation that the existence and presence of the
concept of God—or the overall effect of the existence of a universal moral capac-
ity in the human psyche—created humanity at the “moment” across history when
that universal moral capacity, and the appropriate responses to it, became a reality
within some of our ancestors, and was on its way to becoming a functional poten-
tial within all of us. Perhaps the concept of God was cemented into kin groups all
across the human species as a result of feedback from a spreading grasp of the uni-
versality of the human moral capacity, even if that understanding was never fully
conscious. Perhaps this is the sense in which God (the concept of God) can result
in an unusually broad understanding of universality in humanity.
Anyone taking this view can cheerfully—even enthusiastically—accept virtu-
ally all phrases in which people currently include the term “God” in social cir-
cumstances. Examples are “Thank God,” “God bless,” “In God’s eyes,” “With God’s
help,” or “One nation, under God” (more appropriately, from the reasoning being
promoted here, “One World, under God”—see also terms earlier in this essay). For
example, using the above concepts, it would matter little how explicitly thankful-
ness seems to be attributed to God by an individual for his or her own personal
success in any socially significant activity or competition. Whenever, as individu-
als or subgroups, we invoke or thank a universal God, we would not be acknowl-
edging the will of an entity that for some arcane reason enabled us to win by
favoring us personally over all others. We would be hoping to be acknowledging
or thanking the collective morality and good will of “All the People.” We would be
recognizing the value of the fellowship that characterizes our entire social group,
including, again, “All the People.” We would in a sense be thanking everyone, or
everyone in the group producing or overseeing the particular activity or competi-
tion under consideration. It is surely difficult to fault anyone for thanking a large
number of people collectively for all of their different contributions that happen
to bring about a particular successful outcome. The effect is instead likely to be
heart-warming and reassuring, and I daresay that this is what people who view
themselves as cooperative believers, or who are for other reasons unusually toler-
ant, tend (and wish) to experience in such situations. Thanking God as the spirit
of collective morality would become a unifying and reassuring statement, as it
demonstrates itself, rather than a potentially divisive one implying competition for
favorable attention from a God that in any way bestows special favors on selected
individuals.
The situation just described, though it could include bitter competition
between individuals, teams, or cliques, would not meet the requirements of the
hypothesis being developed here unless it were part of a larger group interaction
that—unlike interactions between individual competitors—could be character-
ized by a potentially over-riding feeling of unity and cooperativeness among its
members. Such a local group would in turn have to be one of several or many
competitive groups. It becomes immediately interesting that this problem of
how social collectives are constructed and maintained, and how such collectives
 Evolution and Religion } 411

interact with each other, is the most important and—for some—potentially dis-
maying consequence of the characterization of God here being described. Yet this
problem is consistent with the failure so far of humanity to succeed in promot-
ing the concept of a unified and universal God theme for all humans—or more
precisely, since all humans live in social groups, for all of the various internally
unified groups of humans on earth.
The apparent match of a large array of terms used traditionally to characterize
God, the nature of which might be called a universal concept of moral capacity
unique to humans, and the additional match between this hypothesis and the des-
perate difficulty in using the concept of God to work steadily toward world-wide
harmony, may alone demonstrate and justify proceeding further with hypotheses
such as those presented here.
I hope it is abundantly clear that I do not seek to disparage the concept of God,
at least when it can be understood in the ways described earlier. I began this pur-
suit with a strong bias that God has to be real in some important (if unusual,
unique, and, with hope, universal) sense, that the most important thing to learn
is precisely what that sense is, and how the concept of God can apply universally,
and merge with the rest of humanity. I also began with a bias that the concept of
God, and the views and approaches that underlie it, are central to human exis-
tence and human endeavors, have been evolutionarily adaptive to the humans
that have appropriated them, and must be clarified if we are to understand our-
selves. Obviously, it is my view that the most useful and acceptable version of God
is universal, and it ought not to be limited to narrow and proscriptive claims.
Nevertheless, considering God as universal raises questions about the likelihood
and effectiveness of any version of our efforts to build and support universal benef-
icence and cooperativeness.

ARE GOD AND EVOLUTION IN CONFLICT?

A Response to The Reverend Gordon Hyslop
I share The Reverend Gordon Hyslop’s feeling (Ann Arbor News, February 14,
2007) that viewing a new baby grandchild is an awesome experience, and that the
human body is indeed a marvel. But one does not have to set the magic and intri-
cacy of human beings against anything at all, as in his statement: “A human life is
a miracle from God, not a process of evolution.” I would like to convince Reverend
Hyslop, and everyone else, that it is not useful to think of God and science as
adversarial to one another.
Our evolutionary background and our religion are together anciently responsi-
ble for both social cooperation and the extremes of social competitiveness, includ-
ing internecine battles that have caused immeasurable pain, misery, and suffering
all over the world. Perhaps, to reduce serious conflicts and expand harmony, we
should join rather than separate our knowledge of evolution and our religious
attitudes and beliefs.
412 { Human Social Evolution

As an evolutionary biologist, I have sought for more than 50 years to under-

stand better how evolution has primed our behavior for particular situations. It
is a difficult problem, partly because much of our knowledge is not automatically
conscious, or has only recently been made conscious. For example, much of what
Reverend Hyslop cites—or can cite—as aspects of human complexity could have
been discovered only within the last few decades by social, biological, and medi-
cal scientists. We became aware of the evolutionary process a mere century and a
half ago, and of genes slightly longer than a century ago. So, unfortunately, it is not
surprising that we like to think that all of our social attitudes and actions are borne
from consciousness, and that genes—as invisible, manipulative, and seemingly
alien forces recently brought into our consciousness—do not in any way influence
how we behave.
Our uses of the concept of God also involve aspects of our makeup that we do
not fully understand. If the concept of God has a real basis—as I believe it must,
because of its virtual ubiquity and the passion we associate with it—then surely
it behooves us to explore everything about the concept and its influences on our
lives, including effects not easily made conscious. Perhaps, rather than continuing
to accept that the concept of God can only refer to a supernatural, anthropomor-
phic, fatherly being, we should ponder straightforward examinations of alternative
ideas about the origin and nature of the concept, its role in the mysteries of the
human mind, and its significance.
For example, what if the power, guidance, and permanence of God derives,
not from a supernatural anthropomorphic being, but from a human-generated
and highly effective use of metaphors referring ultimately to the ancient and
ubiquitous human kin group, and its replacements and diverse forms in mod-
ern society? Thinking of God in our everyday lives evokes primarily emotions
such as love and cooperation. So does kinship, and as well the exchanges of
reciprocal altruism, the risk of net-cost altruism as potential social invest-
ment and return beneficence. God is treated as a concept or spirit, regarded
as a source of strength, authority, morality, and protectiveness. So is the kin
circle and the sociality of the local community. We expect and wish our fami-
lies, or kin groups, to continue indefinitely. So is there an assumption that God
is eternal. To my knowledge none of the approaches to God rejects that, even if
we must attach our affection and our passions through our kin and our collec-
tions of cooperative support. The members of every group, or religion, would
like to think that their particular view of God will eventually prevail, but this
may be true only as long as humanity survives. Members of different groups,
on the other hand, sometimes view God so distinctively that intense competi-
tion and we-they confrontations are prevalent. Both of these attitudes apply
also to our view of kin and benevolent social groups. The desire for wise and
infallible leadership, and the roles of older and more influential individuals
in kin groups—given reluctance to accept death and the value of believing in
communication with deceased leaders or family heads—are possibly long-ago
 Evolution and Religion } 413

facilitators of the envisioning of God as a supreme individual being with powers

beyond our experience in the natural world, including that of negotiating the
prospect of eternal life.
The old “local hubrises” of kin groups and religious groups are indeed enemies
of broader-scale social accord, and they are sufficiently parallel to suggest a com-
mon if not equally ancient background. Local hubris surely has its usefulness, and
not merely in the past. But today’s environment of calamitous destructive pow-
ers—and increasingly rapid and effective world-wide communication and travel—
denies us justification for the destructiveness of continuing regional separatism
and chauvinism—of extreme-we-they confrontations on pride, stubbornness,
economics, politics, religion, kin relationships, unfamiliarity, or even resource
distribution.
Returning to Reverend Hyslop’s microcosm of grandchild effects, the several
adopted grandchildren of my wife Lorrie and myself, whose diverse genetic ances-
tors derive from the far corners of several different continents, have given us con-
fidence that appropriate social learning—assisted by evolutionary understanding
of early imprinting and bonding, and continuing positive association—can yield
the pleasures and strivings associated with kinship as surely and as completely
as do the usual life situations of formally genetic kin. We are fortunate indeed
that the directing of human cooperativeness and competitiveness is largely socially
learned, for such learning, as we know, is subject to manipulation by deliberate
changes in the circumstances of life. No matter how social learning has worked in
the past, knowledgeable application of it in the modern world thus has the possi-
bility of bypassing or minimizing the sometime foibles of our histories with regard
to social and religious variations.
Evolution is not the enemy, even if it has not made us perfect. The sciences we
use to explain evolution—or anything else—are no one’s enemies. Nor is religion,
although it may seem surprising that interpretations of God have seldom led reli-
gious assemblages to bless everyone, everywhere, equally (as noted later, one min-
ister in my childhood church puzzled me, while I was still a child, by consistently
limiting his prayer to, “God bless everyone in this congregation and all those too
ill to attend!”).
Although I am not a fan of supernaturalism, I am also not surprised that others
find it useful or reassuring. Members of my own kin circle rely on a supernatural
concept of God, many of them worshipping in the small country church I attended
as a child, and where Lorrie and I still visit at every opportunity. Our mutual affec-
tion there remains. But for me it is difficult to witness and condone extraordi-
nary and extreme ceremonies, elaborate structures, and assertions that sometimes
channel morality and unsupported impressions narrowly, and even pompously, in
the effort to accept as factual beliefs that supernatural declarations should over-
ride common sense.
I appreciate Doris Lessing’s (1992) insight in African Laughter that, “Myth does
not mean something untrue, but a concentration of truths.” But there is cause for
414 { Human Social Evolution

concern when myth is used as a weapon against other concentrations of truths.

Art, poetry, music, and fiction all utilize myth, and they rarely promote their
business by attacking science. Is it too much to expect that novel and ingenious
cooperative approaches between science and religion can help lessen the world-
wide scourges of unnecessary pain, misery, and suffering, and the continuing sad
parade of deliberately premature deaths from human conflict?

SEEKING GLOBAL HARMONY

Considering Efforts to Alter the World’s Greatest Problem

Try to imagine the complexity of more than seven billion individual humans,
divided among nations and uncountable forms and sizes of groups, all
assiduously pursuing an endless variety and complexity of their separate and
collective interests, and simultaneously trying to think about achieving the
goal of global harmony. Try to imagine the problem of seeking to cause all of
those more than seven billion individuals to remove any significant conflicts of
interest among their various collectives and groupings, or even merely striving
to lessen the worst consequences of their conflicts.
To a large extent, partial solutions to the problem of global harmony depend
today on the governed units termed nations. Organized religions, in different
countries and situations, can also exercise potent influences in the machineries
of nations. Something similar can be said of scientific progress, because
scientists and engineers generate and perfect the paraphernalia of medicine,
business, and much of everyday life, and as well the instruments and practices
of war. As loyal citizens of their nations, and sometimes as staunch members of
religious or other authoritarian groups, scientists can also be influential seekers
of rewards for the creation and use of increasingly horrific weapons of war.
How can we increase the informing of our populations with regard to willingly
competitive and potentially destructive groups in ways that will diminish or
terminate devastating conflicts? How do we escape the hyper-competitiveness
that we all too often praise, beginning with strong advice, praising the most
extreme competitive behaviors to even our young children, as the only effective
route to lifetimes of accomplishment? How do we disentangle ourselves from the
pernicious influence of diversely and competitively sacrosanct hyper-patriotism,
or the divergent and unyielding forms of religions? How do we free ourselves from
the view that our readiness for deadly confrontations outweighs the priceless
value of our military men and women as we hurry to proclaim and cling at
all cost to the sacredness of our essential motherlands? How can we negotiate
and modify governments (and ourselves) to seek successfully the means to settle
conflicts without acrimony, and with an absence, or at least a minimum, of
force or dissension? How, indeed, can we escape from what Abraham Lincoln,
in referencing actions during the horrendous U.S. Civil War, referred to “the
 Evolution and Religion } 415

attractive rainbow that rises in showers of blood”? (Alexander 2011: 286)

Several decades ago I found myself thinking that, in spite of the unique com-
plexity of our brains and our behavior, we humans don’t really know who we are
or how we came to be as we are. The reason, perhaps, involves evolved tendencies
to forget or suppress unpleasantness, and as well be aware of the effects of habit
and non-conscious but well-understood practices and actions (Alexander 2011,
Trivers 2011). As suggested earlier during comments about mysteries, many such
tendencies may be evolved mutings of consciousness, carried out by natural selec-
tion, and scarcely available to the contemplation of most persons or situations. It
seems clear that we have not evolved to wield all of our prodigious mental capa-
bilities freely and effectively. Nor do we seem continually tuned to understand
and contemplate our willingness to engage in serious conflicts that destroy large
numbers of our own people. If we don’t know who we really are, or how to deal
with sometimes galling human extremes, efforts to approach global harmony are
likely to fail. We cannot continue to allow the questions that damp or conceal our
conscious knowledge to pass fleetingly and unmanaged across our minds. This is
why I believe that the most important change that can contribute to global har-
mony is for humanity in general to learn to know itself better, individually and
collectively, as products of our personal backgrounds, including what is derived
from the unambiguous, never-ending process of organic evolution.
Natural selection, the principal force that changes us, tends to move slowly—so
slowly, and sometimes so imperceptibly—that we cannot easily perceive what is
happening or has happened. This has to be one of the reasons for the evolutionary
process and its results being more or less overlooked on an everyday basis. But we
cannot fully understand ourselves unless we are willing and able to examine and
learn how our current life circumstances have come about, and, from that knowl-
edge, how to adjust our lives effectively and profitably. We need to investigate and
lay open our capacity for understanding the ways natural selection has manipu-
lated the patterns of our consciousness, canceled our wayward memories in direc-
tions that favor reproductive success, and prevented, modified, and all too often
warped our potential for the warmth of truly widespread friendliness, empathy,
and cooperativeness. We need to support, to whatever possibilities are reasonable
and available, all of the members of our world and our species.
The manipulations of consciousness that virtually block human
self-understanding, presumably consequences of natural selection, leave us
with an astonishing prevalence of horrific attitudes and behaviors that, sadly,
to many or most people seem either not to exist, or are only moderately and
temporarily noticeable. Team competitions, warfare, genocides, and Beilby
Porteus’s one-murder at a time villains (see earlier) are among the many human
conditions that natural selection has apparently modified by manipulating
consciousness, causing us to respond almost carelessly and forget quickly when
confronted by dramatic and sometimes radical or even monstrous actions of
416 { Human Social Evolution

members of our own species. We seem to live in bubbles of awareness alongside

non-conscious or distortedly conscious strivings, and quick forgetting, the latter
effects products of what Williams (1993) called “The Wicked Witch” of “Mother
Nature”, demonstrating the selfishness of evolution’s differential reproduction
(Alexander 2011, p. 279–80).

It is not an accident that several of the best-known scientists and thinkers in the
history of the world have understood that evolution has been responsible for the
worst of humanity’s activities. Thomas H. and Aldous Huxley, George Williams,
Richard Dawkins, and numerous others have understood that the process of evo-
lution is based on “selfishness,” the “selfish” clustering of the tens of thousands of
genes that build the organisms we become, and as well can follow a course that
mainly generates power and increases access to resources. It would seem that if
humanity is to move toward global harmony, it must modify its fate by understand-
ing our human selves deeply, and by building strong desires and capabilities to
focus on the positive aspects of humanity, reducing the extreme negatives deriv-
ing from hyper-competitiveness and hyper-patriotism, and turning the future of
humanity in new directions concentrated on extensive webs of social investment
and return beneficence—in other words, on the workings of direct and indirect
reciprocity made available by the workings of organic evolution (Hamilton 1964,
Trivers 1971, 2011, Alexander 1978, 1987, 1990, and many others; see note on an ear-
lier page, concerning “altruism”). To accomplish this, we must find ways to over-
come some of the effects of natural selection, and thereby understand ourselves
much more completely, such that we can use all of the knowledge available to us to
serve our own interests.
What else can we do to change ourselves—on a global scale—to reduce our
ever-ready tendencies to compete at nasty levels, or to commit murder, even in
the face of lifetimes in prison or a death sentence; or to wage wars? We surely
cannot lose by striving collectively and mightily toward congeniality and negotia-
tion rather than hyper-competitiveness and conflict, and by seeking reduction of
aggression, using all reasonable means.
These and other suggestions may have positive possibilities. But it does not
seem likely that efforts at such changes will quickly capture our imagination or
yield compelling or worldwide outcomes. It is as if everyone believes that she and
he are already working as hard toward such outcomes as is reasonable or pos-
sible. If that is so, it will not do to expect that the efforts that have been tried so
far can solve the problems. Thus, large numbers of small, local, non-overlapping
groups, socially close-knit and catering to authoritative moral pronouncements,
are unlikely to foster global changes. Such efforts are not likely to solve the prob-
lems because humans have been doing these sorts of things more or less in vain
for thousands of years. Perhaps we can gain by more effectively identifying broad
questions, or knowledge, that can influence a higher proportion of the global
population.
 Evolution and Religion } 417

The greatest difficulty in seeking global harmony may derive from human
groups targeting one another. Humans alone—among all the world’s species—
plot, plan, and organize massive conflicts to defeat or displace similarly organized
and cooperative members of their own species. Can we learn to use the current
consciousness of our human background to adjust team efforts of all kinds so that
honesty, fairness, and negotiation can increase and lead us toward global harmony?
Can we work profitably against the existing minimizing, reversing, and distorting
of conscious knowledge generated by natural selection? Surely such efforts would
contribute positively toward global harmony.
The curious prevalence of wars between conspecific human groups may have
been encouraged by the isolation of human populations that, through extensive
migrations during past millenia, became separated geographically but (thank
goodness!) did not become so different genetically as to prevent increasingly exten-
sive hybridization after establishment of population mixtures. At least among the
distinctive populations forming recently, isolation did not persist long enough to
give rise to different species. But early human populations may not have persisted
in separations long enough to accumulate differences between diverging popula-
tions that increased serious intergroup strife—for example belittling populations
living next to groups different in appearance, language, or cultural patterns (for
a somewhat similar example in much simpler and different hybridizing [insect]
species, see Alexander 2011: pp. 200–201, 205–206). At least during early amal-
gamations of distinctive populations, such differences almost certainly caused
humanity to generate less opportunity and motivation to combine the diversities
of our single species peacefully into mixed populations cooperative against the
array of non-human enemies. Presumably, in some earlier stages of evolution,
humans were still focused almost entirely on non-human enemies. At some point,
humans were surely also less likely, or less well equipped, to treat other humans as
primary enemies. However, as human population sizes increased, and ecological
dominance became a more promising possibility, competition among humans for
resources would have become more concentrated and begun to generate small
closely-knit kin and social groups developing their own rules and desires to con-
test against one another.
Whatever the detailed reasons and timing for the incredible tendencies and
devices that spawn war in modern humans, our current condition, as already
noted, has obviously generated, elaborated, and persisted in supporting massive
and horrific within-species, large-group conflicts, along with serial and copycat
murders, bullying, and other destruction of humans at many levels and in differ-
ent numbers. It is unlikely that these socially negative happenings can be easily or
quickly reversed.
Any route to world peace, or global harmony, surely depends on a relaxed,
tolerant, and unified approach to different attitudes and practices with regard
to social life, religion, and the concept of God and, simultaneously, more criti-
cal attitudes (a) minimizing tendencies to be rigid or authoritarian about local or
418 { Human Social Evolution

group-restricted concepts of right and wrong, and (b) treating more temperately
other groups having different views from our own. I think this because it seems
evident that people everywhere are inclined to invoke some version of God as a
less than universal rallying point, too often in inter-group hostilities, giving us
reason to suppose that in some form religion and God may have been involved in
inter-group adversity for a very long time.
Most specifically, I hope that self-understanding will reveal to us pathways
leading away from our current and evidently historically continuous state of being
a world made up of destructively adverse groups and nations that consistently
invoke religion and the concept of God as inspirations to social unity, apparently
as both conscious and unconscious contributions to efforts to prevail over other
similar groups. Part of uncovering such routes includes recognizing the func-
tion and sometimes dire correlates of intense patriotism, and the warmth and
good feeling that go with the beneficence and cooperativeness that are too often
restricted to within-group interactions.
We are not gentle people. But we can be several kinds of people, depending on
circumstances. In congenial cooperating local groups, we are mostly kin-helpers,
cooperators, and positive reciprocators. When engaging in wars, we frequently,
even if only temporarily, become determined killers.
It will surely take all of the capabilities that humanity can muster to accept
and complement the unpleasant parts of our collective nature, and to minimize
or reverse the unfortunate effects of human history that primed us and set us up
indefinitely to continue threatening extremes of human existence. The world’s
options call for peaceful, casual, and deliberate amalgamations of historically
tiny, introverted, and tightly-knit social groups, and, on the other hand, perhaps
questioning huge nations unable to refrain from becoming armed beyond sen-
sibility. The opposite outcome—the whole world a unified police state—may or
may not be tolerable. Peace may be the goal, but the means and maintenance of
peace will require novel levels of statesmanship and, somehow, continuing floods
of good will.
It would be wonderful if all of humanity could become sufficiently knowledge-
able about its self—positive and negative—to begin to absorb the activities and
attitudes of people living in tightly-knit social groups (whether religious or not),
discovering ways to transform broadly and definitely the cooperative behavior of
the individuals familiar within such groups, along with acceptance of social invest-
ment and the responses of return beneficence on a world-wide basis. To the extent
that these changes can take place, we might find ourselves comprehending how the
building of real cooperativeness and socially positive behavior can turn us toward
a sociality reflecting global peace and harmony.
Many different levels and expressions of consciousness can be involved in
human selflessness, and in compensating both directly and indirectly reciprocal
interactions (Alexander 2011). Promoting the continuance of complex interplay of
social investment and return beneficence in religious and other tightly-knit social
 Evolution and Religion } 419

groups is surely a positive approach to understanding how humans can work

toward global harmony.
Why should we not encourage the diverse people around the earth to be freely
inter-mixed and ready to strive to make all nations democratic—the latter
meaning to attempt reasonable correlates, to call attention to the values of
elections at suitable intervals, personal and confidential voting, multiple voting
political parties, and parliamentary rules and courts that consistently make
democratic institutions work for all people? How can we remove the indefi-
nitely continuing and repeating dictatorships that begin to treat resources as
the property of the government and as a result not only take up war with their
own people but threaten all the rest?

CONCLUSIONS
The several topics undertaken in this essay—religion, group-living, human minds
and mystery, muting of consciousness, science and evolution, concept of God,
meaning of life, explorations of natural and supernatural possibilities, universal or
restricted moral sense, kinship, social reciprocity, competition and cooperation,
and prospects of global harmony—are more than merely difficult. I do not imag-
ine that I have created any broadly credible solutions to the problems I have sought
to disentangle. Nevertheless, entering into searches for the purpose of consider-
ing these difficult topics—or at least calling attention to them—can potentially be
among the worthiest of investigative enterprises.
My effort in this essay has implied that the concept of God arose or became a
dependable spirit of cooperativeness, morality, and beneficence, one that is per-
ceived and acted on within groups to aid and protect the group, either directly or
indirectly against other such human groups, and whether regarded as supernatu-
ralism, or as a natural but jubilant outgrowth of the invisible clouds of effects and
efforts that have generated and persisted out of the stored intellectual mysteries of
the human spirit. Considering the concept of God as a universal spirit of coop-
erativeness within and between social groups should be a repeated and elaborated
effort because it facilitates the evolved function of the lifetimes of individual mem-
bers of the human species, through maximizing the likelihood of persistence of
genes in one’s own genome, ultimately through assistance to those genomes carry-
ing genes in fractions reliably predictable among the relatives making up our kin
groups. Such assistance also involves social investment in unrelated individuals,
including spouses, and partners in social reciprocity, when such assistance eventu-
ally assists own relatives, and may assist all group members whenever individual
and group interests are frequently or permanently similar or identical. The concept
of a universal God, whether it be accepted as metaphorical or otherwise, would
have become possible only with the evolution of a moral capacity, so, curiously,
we might say that God (as the collective expression and coincident awareness of
420 { Human Social Evolution

a universal moral capacity) created humanity, or that humanity created God—or

both— when moral capacity was engendered, directly or indirectly, consciously or
not consciously, by and during the process of organic evolution.
In the sense I have just described them, religion, morality, and attention to the
concept of God are parts of what has been identified as kin selection and direct
and indirect social reciprocity, in which the returns from acts of benevolence can
emerge freely from individuals or groups other than the particular individual(s)
being served. Expanding patterns of social reciprocity and kinship behavior can
potentially continue moving toward global social harmony because they encourage
universal cooperation and fairness (Trivers 1971; Alexander 1974, 1987; Alexander
and Borgia 1978; Frank 1995; Irons 1996a, 1996b; Queller and Strassmann 2009;
Strassmann and Queller 2010).
__________

At the risk of being judged a hopeless megalomaniac, I repeat here that

it is my greatest regret, late in my lifetime of thought and research, that
I have continued to be inadequate in my attempts to discover and explain
how people everywhere might work to understand themselves sufficiently
better from knowledge of evolution, so as to influence the sociality of
global humanity in a positive way. Regardless of the pace of technological
and other scientific advances, understanding of ourselves in evolutionary
terms—understanding sufficiently profound that it requires at least a
temporary ability to withdraw slightly and judge ourselves as if we were
aliens, or members of a different species—may always be necessary if we are
to recognize and accept the most important sources and reasons for change
in the social lives of humans. I regret my inability to identify confidently
even the first steps of a solution to the long-standing central problem of
humanity that derives from the prevalence, throughout our history, of
uniquely ferocious and frequent inter-group competitions, and continuing
elaboration of ever more deadly and dangerous weaponry within our species
(Alexander 2011, slightly altered).
__________
Would that we could shift our attention away from the military, and toward other
countries in the example that Paul Krugman has recently illustrated: “What ails
the Arab world is a deficit of freedom, a deficit of modern education and a defi-
cit of women’s empowerment. So helping to overcome these deficits should be what
U.S. policy is about, yet we have been unable to sustain that. Look at Egypt (cf. the
‘U.N. Arab Human Development Report published in 2002 by some brave Arab social
scientists . . . ’): More than half of its women and a quarter of its men can’t read. The
young Egyptians who drove the revolution are desperate for the educational tools and
freedom to succeed in the modern world. Our response should have been to shift our
aid money from military equipment to building science-and-technology high schools
 Evolution and Religion } 421

and community colleges across Egypt.” (NY Times, and Ann Arbor.com, March
29, 2012)
Why not more such positive efforts that derive from social investment and
the encouragement of return beneficence with the hope of fostering cooperative-
ness and peace, and the potential to establish a gentler and more peaceful world?
Why not?!
_______

It is surely time for the adaptive structures of religion and science

to begin adjusting, finally, into the long-needed partnerships
that can hone their respective capabilities
with the joined skills and emotionalism
of the tangled and still impotent searches
that someday will nurse the gathering fragments
of the potential for global social harmony
alexander, 2011b:312

Acknowledgements

As with all people interested in understanding life, I am massively indebted to

George C. Williams, William D. Hamilton, and Robert L. Trivers, not only for
their fundamental and outstanding publications about how evolutionary selection
works, but for their friendship and their many discussions with me personally, or
in my presence, across several decades. These three biologists are my version of
the most inspiringly original contributors to understanding of the evolutionary
process during the second half of the twentieth century. Each has summarized his
contributions in multiple papers and two or more books. Without their insights
I could not have pursued the meager lifetime agenda I set for myself in 1954, three
years before George C. Williams, and George C. and Doris C. Williams, published
the first two papers developing what I will call the modern view of how adaptation
and the spans of lifetimes work.
With delight and special appreciation, I thank Professor Billy E. Frye, former
Provost of the University of Michigan and subsequently Chancellor of Emory
University, who across several years has been my most important and almost con-
tinual discussant and critic through a range of issues in human evolution, religion,
biology, and many other topics reflected in this current essay. He has taken me
through far too many arguments and corrections for me to remember, including
every major topic involving the discussions in this essay, and as well such unusual
themes as the ins and outs of reforestation, the special lifetime requirements of
orchids and roses, and his unforgettable night-time fox hunts with his father and
other men in the Appalachian Mountains, where Billy grew up and where he now
lives once again, after serving in many different levels of university administration.
422 { Human Social Evolution

Andrew F. Richards and David Lahti have explored with me the topics of this
essay and related others in frequent lunch time free-for-alls across a broad span
of years. Across more than a half century, a succession of approximately 50 doc-
toral students and postdoctoral associates have dealt with all the topics that pre-
ceded this current one during as many years of lunches and graduate seminars.
Numerous other people, including Lorraine Kearnes Alexander, Holly and Paul
Ewald, Michael Martin, Wendy Orent, Naomi Salus, Beverly Strassmann, and
Wesley Upton, are among those who have also reviewed and criticized my most
recent ideas and manuscripts. I am especially thankful to my friends and associ-
ates in the study of human behavior and evolution, William Irons and Napoleon
Chagnon, for aiding me in numerous ways, and across several decades.
Beginning in 2003, members of a discussion group of retired University of
Michigan professors and other personnel (Learning In Retirement), superbly led
by Marlin Ristenbatt, contributed extensively by inviting and re-inviting me to
discuss evolution and religion with LIR, in what turned out to be numerous enthu-
siastic and probing one- and two-hour sessions.
Finally, I am humbled beyond description by the task undertaken by Kyle
Summers and Bernie Crespi, and extremely grateful for the authors who accepted
the tasks of selecting, introducing, and criticizing the chapters of the resulting
volume.

References I
Some of the labels for the concept of God used in this essay were taken from Roget’s
Super Thesaurus, 2nd edition (Cincinnati, OH: Writer’s Digest Books). Otherwise,
some concepts and information used in this essay are widely familiar in biology,
or for other reasons have not included specific references.
Alexander, R.D. 1967. Comparative animal behavior and systematics. In: Systematic Biology.
National Academy of Science Publication 1692:494–3517.
Alexander, R.D. 1971. The search for an evolutionary philosophy of man. Proc. R. Soc.
Victoria 84:99–120.
Alexander, R.D. 1974. The evolution of social behavior. Annu. Rev. Ecol. System. 5:325–383.
Alexander, R.D. 1978. Evolution, Creation, and Biology Teaching. Amer. Biol. Teacher
40:91–107.
Alexander, R.D. 1979. Darwinism and Human Affairs. Seattle: University of Washington
Press.
Alexander, R.D. 1987. The Biology of Moral Systems. Hawthorne, NY: Aldine De Gruyter.
Alexander, R.D. 1990. How did Humans Evolve? Reflections on the Uniquely Unique
Species. Univ. Michigan Museum of Zool. Spec. Publ. 1: iii +38 pp.
Alexander, R.D. 1993. Evolution of the human psyche. In: N. P. Mellars and C. Stringer
(eds.), The Human Revolution. Edinburgh: Edinburgh Press.
Alexander, R.D. 2005. Evolutionary selection and the nature of humanity. In: V. Hosle and
C. Illies (eds.), Darwinism and Philosophy. South Bend, IN: University of Notre Dame
Press, pp. 301–348.
 Evolution and Religion } 423

Alexander, R.D. 2008. Evolution and Human Society. Newsl. Hum. Beh. Evol. Soc. Summer
Issue, pp. 1–20.
Alexander, R.D. 2010. Understanding Ourselves. In: Drickhamer, L. and Donald Dewsbury
(eds), Leaders in Animal Behavior: The Second Generation. Cambridge: Cambridge
University Press.
Alexander, R.D. 2011. The Mockingbird’s River Song: Poems, Essays, Songs, and Stories: 1946–
2011. Manchester, MI: Woodlane Farm Books.
Alexander, R.D. and Gerald Borgia. 1978. Group selection, altruism, and the levels of orga-
nization of life. Ann. Rev. Ecol. System. 9:449–474.
Bigelow, R.S. 1969. The Dawn Warriors: Man’s Evolution toward Peace. Boston: Little, Brown.
Boehm, C. 2003. Global Conflict Resolution: An Anthropological Diagnosis of Problems
with World Governance. In: R. W. Bloom and N. Dess (eds.), Evolutionary Psychology
and Violence: A Primer for Policymakers and Public Policy Advocates. London: Praeger.
Burt, A. and R. Trivers. 2006. Genes in Conflict: The Biology of Selfish Gene Elements.
Cambridge, MA: Belknap Press of Harvard University Press.
Buss, D. M. 2005. The Murderer Next Door: Why the Mind is Designed to Kill. New York:
Penguin.
Darwin, C. 1859. On the Origin of Species by Means of Natural Selection. London: Murray.
Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex, 2nd ed. London:
Murray.
Darwin, C. 1965 [1872]. The Expression of the Emotions in Man and Animals. Chicago:
University of Chicago Press.
Dawkins, R. 1976 (revised 1989). The Selfish Gene. New York: Oxford University Press.
Dawkins, R. 1982. The Extended Phenotype: The Gene as the Unit of Selection. New York:
Oxford University Press.
Dobzhansky, T. 1961. In: J. S. Kennedy (ed.), Insect Polymorphism. London: Royal
Entomological Society, p. 111.
Elkin, S. 1993. Out of One’s Tree. Atlantic Monthly (January), pp. 69–77.
Ember, C.R. and Melvin Ember. 1990. Anthropology. Englewood Cliffs, NJ: Prentice Hal.
Fisher, R.A. 1930 (revised 1958). The Genetical Theory of Natural Selection. New York:
Dover.
Flannery, K. 1972. The Cultural Evolution of Civilizations. Ann. Rev. Ecol. Syst. 3:399–426.
Frank, S.A. 1995. Mutual policing and repression of competition in the evolution of coop-
erative groups. Nature 377:520–522.
Goldhagen, D.J. 2009. Worse Than War: Genocide, Eliminationism, and the Ongoing Assault
on Humanity. New York: Public Affairs.
Hamilton, W.D. 1963. The evolution of altruistic behaviour. Amer. Nat. 97:354–356.
Hamilton, W.D. 1964. The genetical theory of social behaviour I, II. J. Theoret. Biol. 7:1–52.
Hamilton, W.D. 1966. The moulding of senescence by natural selection. J. Theoret. Biol.
12:12–45.
Hamilton, W.D. 1971. Geometry for the selfish herd. J. Theoret. Biol. 31:295–311.
Irons W. 1996a. Morality, Religion, and Human Nature. In: W. M. Richardson and Wildman
(eds.), Religion and Science. New York: Routledge.
Irons, W. 1996b. In Our Own Self Image: The Evolution of Morality, Deception, and
Religion. Skeptic 4: 50–61.
Keith, Sir A. 1949. A New Theory of Human Evolution. New York: Philosophy Library.
424 { Human Social Evolution

Kelly, R.C. 2005. The Evolution of Lethal Intergroup Violence. Proc. Nat. Acad. Sci. 102:
15294–15298.
Lessing, D. 1992. African Laughter: Four Visits to Zimbabwe. New York: Harper.
Queller, D.C. and J.E. Strassmann. 2009. Beyond society: The evolution of organismality.
Phil. Trans. R. Soc., Series B, 364–3155.
Scaruffi, P. 2006. Wars and Genocide of the 20th Century. (http:/www.scaruffi.com/politics/
massacre html)
Strassmann, J.E., and D. Queller. 2010. The Social Organism: Congresses, Parties, and
Committees. Evolution 64-3: 605–616.
Sykes, C. (ed.). 1994. No Ordinary Genius: The Illustrated Richard Feynman. New York:
W. W. Norton.
Trivers, R.L. 1971. The Evolution of Reciprocal Altruism. Quart. Rev. Biol. 46:35–57.
Trivers, R.L. 2011. Deceit: Fooling Yourself the Better to Fool Others. New York: Penguin
Books.
Williams, G.C. 1957. Pleiotropy, natural selection, and the evolution of senescence. Evolution
11:398–411.
Williams G.C. and Doris C. Williams. 1957. Natural Selection of Individually Harmful Social
Adaptations among sibs with special reference to social insects. Evolution 11:32–39.
Williams, G.C. 1966. Adaptation and Natural Selection. Princeton, NJ: Princeton University
Press.
Williams, G.C. 1993. Mother Nature Is a Wicked Old Witch. In: M. H. and D. V. Nitecki
(eds), Evolutionary Ethics. Albany : SUNY, pp. 217–231.

References II: Additional Relevant Books

Armstrong, K. 2009. The Case for God. New York: Alfred A. Knopf.
Atran, S. 2002. In Gods We Trust: The Evolutionary Landscape of Religion. Oxford: Oxford
University Press.
Berger, P.L. 1967 (1990). The Sacred Canopy: Elements of a Sociological Theory of Religion.
New York: Anchor Books.
Boehm, C. 2012. Moral Origins: The Evolution of Virtue, Altruism, and Shame. New York:
Basic Books.
Boyer, P. Religion Explained: The Evolutionary Origins of Religious Thought. New York: Basic
Books.
Chagnon, N.A. 1968. Yanomamo: The Fierce People. New York: Holt, Rinehart, and Winston.
Dawkins, R. 2003. A Devil’s Chaplain: Reflections on Hope, Lies, Science, and Love. New
York: Houghton Mifflin Company.
Dawkins, R. 2008. The God Delusion. New York: Houghton Mifflin Company.
Dennett, D. C. 1995. Darwin’s Dangerous Idea: Evolution and the Meanings of Life. New York:
Simon and Schuster.
Dennett, D.C. 2006. Breaking the Spell: Religion as a Natural Phenomenon. New York:
Penguin Books.
Dennett, D.C. 2011. Science and Religion: Are They Compatible? New York: Oxford University
Press.
Diamond, J. 1997. Guns, Germs, and Steel: The Fates of Human Societies. New York: Norton.
Dunbar, R. 2004. The Human Story: A New History of Mankind’s Evolution. London: Faber
and Faber.
 Evolution and Religion } 425

Gangestad, S.W. and J.A. Simpson (eds). 2007. The Evolution of Mind: Fundamental
Questions and Controversies. New York: The Guilford Press.
Hamer, D. 2004. The God Gene: How Faith is Hard-Wired into Our Genes. New York:
Doubleday.
Harris, S. 2004. The End of Faith: Religion, Terrorism, and the Future of Reason. New York:
Norton.
Hauser, M. 2006. Moral Minds: The Nature of Right and Wrong. New York: Harper Perennial.
Hinde, R.A. 1999. Why Gods Persist: A Scientific Approach to Religion. London: Routledge.
Hinde, R.A. 2002. Why Good is Good: The Sources of Morality. London: Routledge.
Kelly, R.C. 2000. Warless Societies and the Evolution of War. Ann Arbor: University of
Michigan Press.
King, B.J. 2007. Evolving God: A Provocative View on the Origins of Religion. New York:
Doubleday.
Kurtz, P. (ed). 2003. Science and Religion: Are They Compatible? Amherst, NY: Prometheus.
Meisenberg, G. 2007. In God’s Image: The Natural History of Intelligence and Ethics.
Gateshead, England: Athenaeum Press Ltd.
Pinker, S. 2011. The Better Angels of Our Nature: Why Violence Has Declined. New York:
Viking.
Putnam, R.D. and D.E. Campbell. 2010. American Grace: How Religion Divides and Unites
Us. New York: Simon and Schuster.
Rue, L. 2005. Religion Is Not About God. New Brunswick, NJ: Rutgers University Press.
Shank, N. 2004. God, the Devil, and Darwin: A Critique of Intelligent Design Theory. Oxford:
Oxford University Press.
Shermer, M. 2011. The Believing Brain. New York: Henry Holt and Company.
Taverne, R. 2005. The March of Unreason: Science, Democracy and the New Fundamentalism.
Oxford: Oxford University Press.
Trivers, R. 2011. Deceit: Fooling Yourself the Better to Fool Others. London: Penguin.
Wade, N. 2009. The Faith Instinct: How Religion Evolved and Why It Endures. New York:
Penguin.
Wilson, D. S. 2002. Darwin’s Cathedral: Evolution, Religion and the Nature of Society.
Chicago: University of Chicago Press.
Wright, R. 2009. The Evolution of God. New York: Little, Brown and Company.
15 }

Evolution and the Arts

Creating the Treasures of Your Truths and Mine

Science begins with ideas from observations:
builds scenarios that thrive on journalistic directness.
Its novelties are newly known theories and facts,
the best of them robust, unalterable,
crammed with promises of broad significance
for everyone, said to be valuable
because of objectivity.
Art begins with ideas from observations:
builds scenarios that thrive on metaphor and mystery.
Its novelties are sublime and outrageous:
take-it-or-leave-it, the best of them
boundlessly interpretable, accepted as subjective,
crammed with promises of personal meanings
for everyone, said to be valuable
because of subjectivity.
Science—formal and informal—establishes
the successions and progressions of realities
on which the continued elaboration
of both science and the arts depend.
The mental capacities and tendencies that
facilitate the practice of art,
and render it joyous,
facilitate science as well,
and render it also joyous.
Realities deriving from use of the imagination
in either science or the arts—or merely life—
may seem personal to the scientist or the artist
at every stage.
 Evolution and the Arts } 427

Realities derived from use of the imagination

in the arts are saved or accepted by personal choice
from the beginning,
can be rejected at will,
and also personally.
Realities deriving from use of the imagination
in science sometimes seem alien,
especially to the populace on which
they are necessarily imposed,
rather than merely invited or sought.
Science and the arts together
enrich the imagination,
imagination drives discovery,
discovery builds knowledge,
knowledge enriches lives.
Art and science each offer novel truths,
foster enthusiastic or fearful incredulity
over the richest of their contents:
one discovered via repeatable hence verifiable
procedures, a tearing down to rebuild further,
on more solid ground, the other on faith
via trust in unrevealed procedures, trust
imposed or accepted as a result of differentials
in the strength of human authority;
sets of truths valued either similarly by all
because they apply to interests common to all,
or offering diverse usefulnesses,
enhancing separately
the unique interests of individuals.
Science progresses with great difficulty
toward explanations of such as meanings,
emotions, likes and dislikes—
so far has tended to resolve problems
largely at physical or physiological levels,
through procedures thriving on reduction and
dissection, to levels conducive to analysis,
followed by slow reconstruction
toward admired and desired wholes.
428 { Human Social Evolution

Art exposes and creates novelty

in personal and emotional propositions,
often at their own level, seeking insights
more through sense-expanding meanings
than through sense-extending technologies.
The novelties of science and the arts
contribute to all our prospects,
adjusting physical and social possibilities,
extending personal and social meanings.
Alexander, 2011, p. 257
 INTRODUCTION

Cornerstone to Capstone: Richard Alexander on Social Selection

and the Arts
Kyle Summers and Bernie Crespi

(An introduction to an excerpt (Pp. 333–345) from Alexander, R.D., 2008.

Evolutionary Selection and the Nature of Humanity, Pp. 301–348 In. (V. Hosle and
C. Illies, eds.): Darwinism and Philosophy, University of Notre Dame Press, Notre
Dame, IN.)
Evolutionary understanding of human behavior was grounded in scientific inquiry
by Darwin’s (1859) theory applied to the “necessary acquisition of each mental
power and capacity by gradation” in his novel process of natural selection. Among
all human capacities and achievements, the arts stand alone as furthest from our
primate roots, and apparently least amenable to explanation by step by step natu-
ral selection and gradation. As such, the arts, as pinnacles of human achievement
with no apparent basis in adaptive function, represent an exceptional challenge
to theories of how humans have evolved. For these reasons, we consider Richard
Alexander’s contributions to penetrating the evolutionary underpinnings of art
as one of his crowning achievements—an achievement that makes clear his entire
framework of thought, from foundations in selection of gene and individuals to
capstones in mental powers and capacities that are uniquely human.
Human striving in the context of the arts is one of the most impressive yet puz-
zling examples of human uniqueness. While tool-making—and hence primitive
technology—can be found in many animals, artistic endeavor seems considerably
more restricted in its taxonomic distribution. Some animals have created what
humans call “art” under artificial circumstances (Morriss-Kay 2010), but there is
no scientific evidence that these creations are in any way equivalent to human
artistic creations (Zaidel 2010). How has capacity for art evolved—or more spe-
cifically, what processes of variation, heritability and, most importantly, selection,
could have led to the gradual evolution and maintenance of a human trait at least
as unique as language, but apparently much less directly useful?
The evolution of human artistic capacities and skill has remained, until very
recently, a surprisingly neglected topic (Dissanayake 1992 Aiken 1998; Boyd 2009;
Dutton 2009). Two recent overviews provide insights into current opinion on the
430 { Human Social Evolution

evolution of art. First, Moriss-Kay (2010) gives a historical perspective on the evo-
lution of art in the hominid lineage, tracing its development back hundreds of
thousands of years. Although art has commonly been held to have appeared less
than 45,000 years ago with the migration of modern Homo sapiens from Africa
to Europe (e.g., Bar-Yosef 2002), Moriss-Kay (2010) argues that the earliest evi-
dence for art far predates this event. She takes a broad view of what constitutes art,
including body decoration using pigments. Evidence for human artistic creation
has been found from as long as 164,000 years ago, from recent excavations of caves
in southern Africa (e.g., Jacobs et al. 2006). These excavations have revealed a
variety of traces of artistic endeavors, including color pigments (likely used for
self-decoration), engraved bones and decorative beads. Hence, while the flower-
ing of artistic creativity seen in the abundant art created by early European Homo
sapiens may indicate important changes in human artistic abilities, the evolution
of art is likely to have much deeper roots in the hominid lineage. These studies
provide important descriptive context for the origins of art, but tell us nothing of
why individuals creating or wearing adornment presumably outreproduced those
who did not.
Second, Morriss-Kay (2010) points out that early European cave painting,
which many researchers find the most striking example of prehistoric art, focused
on animals that are either hunted (e.g., bison) or hunters (e.g., lions). These ani-
mate artistic subjects suggest functions associated with the observation of, and
reverence for, prey species, and admiration and emulation of effective hunt-
ers (particularly cooperative group hunters such as lions). She argues that early
European art emphasized key components of sociality such as group cohesion,
kindness and parental care on the one hand, and hunting skills on the other. With
respect to the latter, she suggests that a key function of art—leading to its evolu-
tion—was the importance of the development of the “mind’s eye,” allowing early
humans to visualize the final product of tool construction when beginning with an
block of unworked material (such as a rock), or allowing hunters to visualize the
location of prey even when they have disappeared from current view. Hence, she
follows a long tradition of viewing art as a functional extension of human tech-
nological capacity, particularly in the context of hunting (e.g., Heinrich 2001). But
if art indeed originated in functionally based visualization, what drove the initial
transition, and later transformations to arbitrary form?

SEXUAL SELECTION OF THE ARTS

One ultimate explanation for the evolution of art focuses on the idea that art evolved
as a display, closely connected to courtship and mate selection in the human lin-
eage (Zaidel 2010). A number of authors (e.g., Zahavi & Zahavi 1997) have likewise
proposed that a key function of art, and other manifestations of cognitive com-
plexity, manifests in its contributions to success in sexual selection. For example,
some researchers have focused on the potential relevance of Zahavi’s Handicap
 Evolution and the Arts } 431

Principle in explaining artistic accomplishment as a—signal of the underlying

“cognitive quality” of the artist (including Dr. Zahavi himself—Zahavi & Zahavi
1997). Perhaps the most well known advocate of the importance of sexual selection
in the evolution of artistic ability (and many other aspects of human intelligence,
including language) is Geoffrey Miller. Specifically, Miller (2000) argues that artis-
tic creativity evolved to create displays that were evaluated by members of the
opposite sex in the context of mate choice.
A key limitation of this approach is that it focuses on male-male competition.
Presumably, under this argument, the evolution of artistic abilities in females is
an epiphenomenon of the operation of selection on males, rather like the occur-
rence of horns in females of some species of ungulates (Lande 1980). Strong sexual
selection is typically associated with extreme sexual dimorphism (e.g., Andersson
1994), and hence one might predict extreme sexual dimorphism in intellectual
and artistic abilities, which does not accord with a substantial body of data (e.g.,
Charyton et al. 2008). However, Miller (2000) emphasizes that mutual mate choice
was likely to be the rule rather than the exception over the course of human evolu-
tion, and hence sexual selection could favor similar traits and levels of expression
in both sexes simultaneously. He argues that three different forms of sexual selec-
tion, including Fisherian Runaway, sensory biases and good genes indicator mech-
anisms, are all likely to have contributed to the evolution of artistic creativity and
abilities (and other human mental attributes), but that indicator mechanisms are
likely to have comprised the dominant mechanism over the course of human evo-
lutionary history. For art in particular, Miller (2000) argues that the good genes
hypothesis is particularly appropriate to explain the apparent luxuriant extrava-
gance that seems to characterize many forms of artistic creativity and expression.
Miller’s arguments have attracted a substantial amount of attention, both posi-
tive and negative. On the positive side, several authors have taken his ideas to
heart and expanded on them. For example, Dutton (2009) presents Miller’s argu-
ments as the most likely explanation for the evolution of artistic ability in his
recent book on the evolution of art. By contrast, others (e.g., Driscoll 2006) have
criticized Miller’s conclusions on several grounds. For example, the claim that art
always or even usually functions as a courtship display does not stand up well
to scrutiny. Also, art is not always aesthetically pleasing in the way that Miller
predicts, and indeed great art sometimes deliberately flaunts notions of aesthetic
pleasure. Further, Miller’s “sexual equivalence” argument posits that men have
preferred artistically talented women as mates throughout human history, but he
does not present convincing evidence for this criterion of mate choice, in either
historical or current human populations. Miller also makes a secondary argument
for a “producer-consumer” relationship between men and women in the context
of artistic ability, but this argument simply throws us back to the prediction that
there should be sexual dimorphism in artistic ability between human males and
females.
432 { Human Social Evolution

If sexual selection cannot substantially or completely explain the origin and

evolution of art, might we default to considering it a Gouldian spandrel of selection
in some other context, as Dawkins conceives religion? For example, Steven Pinker
(1997) has argued for art as a kind of epiphenomenon that arises from having a
brain highly adapted in the context of technical problem-solving. Artistic creativ-
ity and skill would hence have no ultimate adaptive value. But why, then, would
they remain universal across human cultures, costly in terms of energy, time and
resources that could be devoted to more fitness-increasing functions, and notably
pleasurable, like so may other adaptive phenotypes (Dissanayake 1992).

SOCIAL SELECTION OF THE ARTS

The work of Richard Alexander on the evolution of artistic creativity provides an
original, rich, complex and compelling alternative to the hypotheses reviewed
above. Alexander first wrote about the evolution of art in several classic works on
human behavioral evolution (e.g., Alexander 1979, 1987), and more recently has
expanded on the importance of social selection—selection caused by mutualistic,
competitive and exploitative social interactions within a species, whereby the same
individual can play multiple roles, such as recipient, donor, or observer of social
actions—in understanding the evolution of human artistic capabilities (Alexander
2008). These works appear to have gone largely unnoticed by most researchers in
this field. Indeed, as Alexander (2008) points out, most of those who write about
the arts do not consider its evolutionary foundations at all (e.g., Barzun 2000).
Alexander (2008) begins by warning that the ultimate explanation of the arts
that he is proposing is likely to be highly objectionable to many people, because
it focuses on the effect of artistic endeavor and accomplishment on the inclusive
fitness of the artist and the observers of artistic creations. In the context of human
societies, in which cooperation is highly prized and selfishness is considered a
fundamental character flaw, the notion that we are, in large part, motivated by a
desire to contribute to the general welfare of society is very strong (in and out of
academia—see for example Gintis et al. 2003).
Alexander’s work on the arts is grounded in the concept that the ultimate goals
of human striving—in maximization of inclusive fitness—are normally hidden
from us. He emphasizes that it is specifically because our motivations are more
selfish than we would like to admit—lest our selfishness be used against us in the
continual struggle to form and maintain cooperative alliances—that it is so dif-
ficult for us to perceive or accept them. Indeed, Alexander (1989) has argued that
the elaborate structure of consciousness, with multiple layers, many of them hid-
den, evolved in part to keep our true motivations obscure, allowing us to proceed
in our daily lives fully convinced of the underlying selflessness of our true motiva-
tions. This kind of “self ” deception—or lack of conscious awareness of underlying
motivations—can be useful in enabling success in the arena of social competition,
as also emphasized by both Trivers (1971) and Alexander (1979). Hence, we have
 Evolution and the Arts } 433

evolved a multi-layered and modular consciousness in which our own ultimate

motivations are well hidden, even from ourselves. As Alexander argues, our per-
ception that artists are motivated by “pure” striving for perfection should not deter
us from seeking an ultimate explanation. Such considerations, of course, apply
much more generally to the evolution of human mental powers and capacities, and
may motivate non-evolutionary spandrel-based “explanations” of art, religion, and
other difficult to explain arenas of human behavior and cognition.
Human motivations and striving are fundamentally social, yet human societ-
ies are unusual among animals in the high degree of autonomy of their members
(Alexander 2008). Unlike genes in a genome, our reproductive success is often not
closely bound to that of other members of the group. Unlike the members of social
insect colonies, or groups of cooperatively breeding vertebrates, we are geneti-
cally unrelated to the vast majority of the other members of our societies. Recent
research emphasizes the point that this social-genetic structure has persisted for
much of our evolutionary history (Hill et al. 2011). Such autonomy makes the opti-
mal strategies to pursue in negotiating the complex balance of cooperation and
conflict, within and between the multiple levels of hierarchy within and between
societies, more difficult to perceive and accomplish. Overlaying the fact that our
true motivations are effectively hidden from us complicates the task even further.
Nevertheless, humans are highly accomplished at evaluating the costs and ben-
efits of pursuing a huge number of possible courses of action, particularly as they
relate to social outcomes. Such evaluations involve forms of more or less conscious
“scenario-building,” whereby behavioral options can be explored safely within the
mind, as a core adaptive function of the human psyche (Alexander 1989).
How do human cognition and sociality relate to the arts? As Alexander (2008)
emphasizes, the arts embody elaborate forms of scenario-building, and he places
the importance of such scenario-building firmly in the context of the unique
nature of human societies, in which close cooperation and mutual dependence are
coupled with an over-arching lack of close genetic relatedness between cooperat-
ing individuals. Competition and cooperation, under varying degrees of mutual
dependence, are thus inextricably mixed. Scenario-building—in the minds of self
and others—has led the arts to achieve a level of importance in human societies
that makes it possible for successful artists to pursue their art exclusively and be
well compensated in turn by those who would like to enhance their own scenario-
building and executing skills through observation of the works of a master. Hence
the arts, far from representing some sort of trivial pursuit, embody one of the
highest levels of intellectual achievement available to our species. Ironically, the
extreme importance granted to the arts in many cases transforms them from mere
practice to the main event itself—as any parent of a child in a play can attest.
Alexander (2008) develops the concept of artistic endeavor as a key compo-
nent of social and intellectual play in the context of striving for inclusive fitness
returns via self-improvement. This conception of art focuses on the paramount
importance of scenario building as part of skill development and task completion,
434 { Human Social Evolution

and parallels the focus on the development of the “mind’s eye” discussed above.
Unlike other researchers, however, Alexander emphasizes the supreme impor-
tance of visualizing social relationships, of visualizing the effect of one’s own
strategies in the context of the strategizing of the multiple others that influence
one’s fitness in human society. For an evolutionarily significant period of time,
the unique ecological dominance of the human species makes this social milieu
the key arena in which the inclusive fitness of individuals has been determined in
human societies. Given the complexity of evaluating the possibilities and choosing
the best course in an intricate array of possible courses of action, the importance
of scenario-building cannot be over-emphasized as a key component of social suc-
cess. As Alexander (2008) argues, this is particularly true given the relative nature
of success in human societies, and the fact that all other members of society are
continuously updating their scenarios on the basis of those of others, and attempt-
ing to take advantage of that information. In this sense, human scenario-building
generates positive feedback loops that drive accelerating increases in both social
and cognitive complexity (Crespi 2004; Flinn and Alexander 2007).
Alexander (2008) recognizes two aspects of the arts. First, art is used as a means
to promote an individual’s striving for success within society by enhancing their
own physical and mental talents in the context of the elaborate creativity, plan-
ning, scenario-building and performance execution required of artists. Second,
arts generate potential value to the observers. Observers of artistic creations and
performances can obtain a variety of benefits relevant to their own striving in the
context of mental scenario building and related activities. Such gains are particu-
larly salient in our species given our unique capacities and proclivities for cul-
tural transmission (Richerson and Boyd 2005). As Alexander (1979) has argued
in detail, culture is not a neutral medium, but rather the key setting within which
human striving takes place. Cultural adaptations are created and maintained by
the considered or unconsidered imitation and anti-imitation of the behavior of
members of society (particularly successful members) by other members as they
strive to enhance their own status within the social hierarchy (Alexander 1979;
Flinn and Alexander 1982). This approach presages similar arguments made by
researchers focused on gene-culture coevolution (e.g., Richerson and Boyd 2005).
Art, as the embodiment of cultural traditions that take on enduring importance
across generations in human societies, constitutes a fundamentally important
arena for competition to succeed in the social hierarchy in human social groups.
Hence the task of learning the nuances of these traditions—specific to particular
societies—from those who have mastered them becomes of paramount impor-
tance if one is even to play the game, never mind succeed in it.
Alexander (2008) places the unique importance of artistic endeavor and
achievement squarely in the context of his well-developed view of ethical and
moral behavior within human societies (e.g., Alexander 1979, 1987). Specifically,
he conceptualizes human societies as networks of direct and (largely) indirect reci-
procity, in which it is critically important to maintain and enhance one’s reputation
 Evolution and the Arts } 435

in the eyes of other members of society. Members of society are constantly observ-
ing and evaluating all other members, rewarding those who contribute to society
and punishing or shunning those who act to the detriment of the common good.
These unique levels of social cooperation take place in (and are driven by) the
importance of intergroup competition that make cohesive, cooperative groups the
most likely to survive and succeed over the course of human evolutionary his-
tory (Alexander and Tinkle 1968; Alexander 1979, 1987). These arguments have
(belatedly) been supported via modeling and empirical analyses by a variety of
evolutionary anthropologists, economists and psychologists who have recently
taken an interest in this area (e.g., Choi and Bowles 2007; Boyd et al. 2009). Scant
explicit acknowledgment has been accorded to the pioneering contributions made
by Alexander in this domain—partly through specialization and ignorance, but
perhaps also because Alexander’s perspectives, through his works and those of
his students and colleagues, have become so deeply and thoroughly embedded in
ways of thinking as to escape conscious notice and citation.
Reputation and status within society thus take central places in Alexander’s
(2008) explanation of the evolution of artistic creativity and ability in human soci-
ety. Status is always relative and always in short supply, and high status is accorded
to those who can demonstrate exceptional abilities of perception, appreciation,
interpretation, translation, and communication via their artistic talents. These
traits qualify them, in the eyes of multiple observers, to distill, amplify, and express
essential features of the social system through their art. In turn, the ability to appre-
ciate the subtle nuances of artistic performances also requires exceptional abili-
ties of perception and interpretation on the part of observers. The ever-increasing
complexity of the interaction between the performer and the observers that char-
acterizes the arts provides an open-ended arena for intellectual play that hones the
scenario-building capabilities of both performers and observers, both within the
lifetime of particular individuals and across the generations in human societies.
Alexander (2008) takes care to distinguish the process of social selection from
sexual selection. Partners in social selection can alternate roles or assume the same
roles in their interactions, which center on mutually beneficial forms of direct or
indirect reciprocity. These interactions form the main fabric of human society and
involve long-term investments in relationships with the potential for both high
risk (due to cheating) and high long-term reward. Staying “one step ahead” in such
relationships becomes paramount, leading to selection in favor of extraordinary
capacities in the realms of social observation, memory, communication (linguis-
tic abilities), empathy, sympathy and other components of scenario-building that
form the basis for what we call consciousness. These capacities allow us to be aware
of our own thoughts and intentions, to communicate them effectively, to be cog-
nizant of alternative courses of action available to us at different times and places
in the future, and to act in our best interests in response to those contingencies.
The term “social selection” implies that the expression and appreciation of
artistic creativity ultimately affect the inclusive fitness of the individuals involved,
436 { Human Social Evolution

and Alexander (2008) carefully explains how artistic endeavors may connect to
heritable traits associated with reproductive consequences. He first reiterates pre-
vious arguments (e.g., Alexander 1979) that the learned behaviors comprising
culture are not independent of the impact of selection during our evolutionary
history, but rather that we have inherited myriad biases, tendencies and capacities
that regulate how experience affects learning, which behaviors are adopted (and
from whom), and how those behaviors are expressed. Hence culture and cultural
transmission are profoundly affected by inherited biases and capacities, which are
in turn subject to selection. Rather than being independent, genetic and cultural
evolution are linked and influence one another in a reciprocal manner (Richerson
and Boyd 2005). The extreme phenotypic plasticity associated with learning makes
it appear that activities that require long periods of training and practice (such
as art) are independent of any innate variation in ability, but this is not always
the case (Ebstein et al. 2010). Heritable traits influencing artistic proclivities and
abilities may be specific, or may reflect general overall attributes such as health,
immunity, processing efficiency, etc. that can provide a substrate for excellence
in the arts as well as other endeavors. Indeed, Alexander (2008) also makes use
of Zahavi’s Handicap Principle in this context, such that general capacities may
underlie the ability of performers to succeed in artistic endeavors. Artistic creativ-
ity and capability may thus serve as markers for underlying characteristics that are
desirable in a social or sexual partner, such as intelligence and empathy.

RUNAWAY SELECTION AND THE ARTS

Like Miller (2000), Alexander (1987, 1989, 2008) has accentuated the possibil-
ity that some form of runaway selection may have contributed to the tendencies
toward extremes seen in artistic endeavors and competitions. Unlike Miller, how-
ever, Alexander focuses on runaway selection in the context of social competition
rather than sexual selection. The possibility of runaway social selection has been
discussed for some time (e.g., West-Eberhard 1983; Nesse 2007), but few attempts
have been made to model this process formally. As Alexander (2008) points out,
systems of direct and indirect reciprocity may be particularly appropriate vehicles
for the action of runaway social selection that operates in a manner parallel to that
originally suggested by Fisher (1930) for runaway sexual selection.
Two properties may make the comparison of social with sexual runaway selec-
tion appropriate: (1) the tendency to choose extremes (to pick the best mate in
sexual selection, and the best partner in systems of reciprocity), and (2) feedback
between the benefits of choosiness to the chooser and of being chosen to the
performer. These features may drive the competition to extremes, whereby the
(original) practical nature of the performance is lost as performers seek to exag-
gerate their art in an attempt to achieve the most extreme performance. In turn,
observers may come to appreciate the extremes, not for their practical useful-
ness, but rather as markers of the extreme capabilities of the performers. This
 Evolution and the Arts } 437

kind of process can occur with or without underlying heritable variation in ability
and appreciation, as winning performances may yield direct material benefits for
both the performers and the observers. Alexander (2008) discusses fascinating
examples of artistic and other types of competitions that have followed bizarre
and unique trajectories. For example, in horse-riding competitions, the contrast
between “peanut-rollers” (where the horse’s head is held low during the ride), and
the opposite, where the horse holds both its head and body extremely high, illus-
trate opposite trends that have both gone to extremes. These competitions have
led to extremes that are in no way functional, but allow observers to judge which
participant has achieved the most extreme result (and accord status as a result).
The proliferation of these kinds of competitions, both in the arts and in sports
and other components of human society, has been remarked upon by generations
of observers.
Distinct competitive races, in the arts and elsewhere, may arise in a diversity
of contexts, at a number of different levels in the social hierarchy, and of course in
different societies. These properties vastly increase the number of opportunities
for individuals to fruitfully engage in artistic competition, by choosing compe-
titions that are appropriate to their specific type and level of training, skill and
opportunity. As Alexander (2008) points out, these considerations, in combina-
tion with the tendency to favor extremes in such competitions, may have lead to
the diversity of artistic pursuits we see today.

NATURAL SELECTION, THE ARTS, AND UNDERSTANDING HUMANITY

Our brief history and synopsis of Richard Alexander’s contributions to under-
standing the arts serve not just to introduce his contributions in this area, but also
to exemplify his incisive and comprehensive manner of thinking about natural
selection in human evolution. One cornerstone, inclusive fitness theory, anchors
human evolutionary biology from genes to brains, and connects competition with
cooperation across all human endeavors, including the arts, its most exceptional.
Indeed, understanding Alexander’s arguments and hypotheses regarding sexual,
social and runaway selection of the arts compels an understanding of his entire
perspective on understanding ourselves. In turn, his ideas, which generate testable
predictions that interface across scientific disciplines from genomics to neurosci-
ence and anthropology, should motivate and inspire the next generation of studies
in evolution and the arts.

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 EVOLUTIONARY SELECTION AND THE NATURE OF
HUMANITY

Excerpt from Alexander, R.D. 2008. Evolutionary Selection and the Nature of
Humanity. In: V. Hosle and Ch. Illies (eds.), Darwinism and Philosophy. South
Bend, IN: University of Notre Dame Press, chapter 15.

Connecting the Arts to Evolution

People who are successful in the arts possess a set of basic skills that they use in
relation to the social scene: observation, perception, appreciation, interpretation,
imagination, prognostication, translation, and communication. They depict the
social scene through faithful representations mixed with manipulation, exag-
geration, and the parading of incongruity—all of which require extraordinary
ability to understand the social scene in the first place. They use visual portray-
als in art, dance, and drama. They use language in all forms, from oral narration
and music to the literature of poetry and fiction. They use metaphor in every
sense of the concept, and the race to catch up with all of the ways they do so
will never be finished. They use humor, and to those who are sufficiently atten-
tive they demonstrate its deadly seriousness. They combine most or all of these
media, sometimes in a single stunning performance that creates novel compari-
sons and portrays relationships that enlighten and explain the social world as
never before.
Audiences of the arts are accepting particular versions of the social scene sec-
ondhand from others whom they perceive to have better basic skills or broader
experience. To do this effectively they must recognize the relevant talents and abil-
ities in others. Basic to that task are universal and special features of the human
brain: social capacity that includes a fertile imagination and all the talents neces-
sary to use it. These traits are the same as those employed by the artists, leading
us to wonder if they derive from a single machinery, even if not always equally
functional.
The result of all this is that the arts are a glorious form of interpretive gossip,
multifaceted, multilayered, and altogether still complex beyond anyone’s compre-
hension. People in the arts are by definition the best storytellers among us. What
they tell us is never superfluous, impractical, or trivial unless we, the audiences,
allow it to be. We gain mightily from knowing how and when to listen, to whom to
listen, and what to do with the experience afterward. For the arts are theater, and
theater in all of its guises represents the richest, most condensed, and most widely
 Evolution and the Arts } 441

understood of all cultural contributions to our patterns of social scenario build-

ing through consciousness and foresight. These scenarios, which we build, review,
and revise continually every day of our lives, are obligate passports to social suc-
cess, and perhaps the central evolved function of the human social brain. We use
them to anticipate and manipulate the future—the ever more distant future in ever
greater detail.
When Marshall Sahlins (1976) argued that modern hunter-gatherers are mod-
els of the original affluent societies because of the surprisingly small amounts of
time spent hunting and gathering, he underplayed at least two things. First, time
not occupied with securing food and shelter can only be occupied otherwise; and
this can be done effectively only by engaging in activities that contribute to repro-
duction. Second, sitting around being social is not necessarily trivial or nonrepro-
ductive. Sahlins’s comments, however, emphasize that the rise of art in its various
expressions need not be restricted to recent societies demonstrating leisure time
and affluence in some narrow modern sense.
Even if few could say it as well as Doris Lessing (1992, 35), artists are the people
who understand that “[m]yth does not mean something untrue, but a concentra-
tion of truths.”

Status and the Arts

Status is central in human society (cf. Barkow 1989; Dickemann 1979; Henrich and
Gil-White 2001; Hill 1984). It is important to every individual in society, hardly
ever approaches being “complete,” and by its nature is always in short supply. For
humans, unlike any other organisms, the numbers and kinds of differences in sta-
tus in a complex society can be almost endless and constantly changing; in today’s
societies, one individual can have different kinds of status in numerous different
social circles. These facts create endless and elaborate performances and audi-
ences, as well as endless opportunities and competitive races leading to narrow
trends and fads about which little more can be said beyond “Second place is the
first loser.” These things happen because, for various reasons (see below), audi-
ences to artistic performance and competitive races can sometimes gain as much
as or more than the participants. I would be surprised if any species has anywhere
near as many performance-audience interactions as humans.
If status is, as seems evident, a measure of access to the resources of reproduc-
tion, we can grasp the importance of understanding it, and how to gain it, in a
society like our own. How and why status has become so important in human
society is another question. It can be complex and dynamic only when indirect
reciprocity has become important. Reciprocity and nepotism are both investments
that entail risk. Only a genetic return is required to make nepotism profitable, and
unlike social reciprocity, much nepotism can occur regularly with a minimum
of cognitive skill. Differential nepotism frequently takes the form of reciprocity,
442 { Human Social Evolution

however, when two relatives reciprocally assist one other in times of special need
for first one, then the other (see discussion in Alexander 1979a, 53–56). Success in
reciprocity, with the simultaneous retention of social acceptance and harmony,
requires the highest levels of cognitive skills (see, e.g., Trivers 1971).
From these assumptions it would appear that the underlying reason for direct
reciprocity, followed by indirect reciprocity and an importance for status shifts in
human society, is actually group living of the sort discussed earlier, which allows
and promotes the kind of extensive differential nepotism apparently unique to
humans and the most likely precursor of reciprocity.
The existence of status as an important variable in human society sets the
stage for interest in any kind of contest or performance that assists in determin-
ing status accurately and in changing it to the observer’s or participant’s benefit.
In Alexander (1979a), I hypothesized that much of the arts represents surrogate
scenario building for audiences. I have also suggested previously that, for per-
formers, all of the arts can provide opportunities for the elevation of status. Status
and the ability to convey items of great importance to others go together. They
may represent the key to understanding not only the arts but much of morality as
well, because lowered status is effective punishment for behavior deemed immoral
(Alexander 1987). Part of the reason this is possible, of course, is that coalitions
and alliances capable of meting out punishment, as well as delivering rewards,
can form within human groups and are aspects of indirect reciprocity. It is a large
part of the complexity of human social life that, as part of the group-against-group
aspect of human sociality, these coalitions can also shift and change in virtually
every way imaginable.

The Contribution of Social Selection to Human

Culture: Is It a Runaway Process?

We need now to engage more specifically the question of the particular flow-
ering of the collective human phenotype usually called “culture.” It is obvious
that extensive learning abilities in humans, and the long and intimate overlaps of
adults and juveniles in social groups, have created a situation in which learned
activities are transmitted by learning, thus providing the background for the
rapid accumulation of cultural innovations and change, consequently for rapid
cultural divergence among variously isolated human groups. But without addi-
tional explication these facts seem frustratingly unable to account for the incred-
ible races toward complexity and diversity of human social and cultural activities
across the globe—not only the huge specialized human brain but the features
that have led to such complex and diverse enterprises as the arts and, indeed,
those leading to Barzun’s (2000) label of decadence. Something more is needed—
another step in our understanding of evolutionary process—to connect every-
thing about the human organism to its complex cultural expressions. I ask now
 Evolution and the Arts } 443

whether this “something more” may be considered appropriately under the label
of runaway social selection, already introduced in this context by West-Eberhard
(1983) and Alexander (1987, 1989).
Ronald A. Fisher (1930) used the adjective runaway to apply to a hypothetical
selective process that he assigned to sexual selection (see also Trivers 1972; Miller
2000). I suggest that sexual selection and reciprocity selection are special forms
of the broader concept of social selection. Social selection is a consequence of
competition among individuals for rewards arising out of various kinds of social
or mutualistic beneficence.
Fisher’s runaway sexual selection has two special features. First is the tendency
of the choosing parties to begin favoring individuals with traits that are extreme
on some axis of desirability, rather than favoring some particular condition (other
than extremeness) of the individuals to be chosen. This form of choosing can only
occur in an organism that is able to compare an array of individuals and iden-
tify desirable extremes (e.g., Alexander, Marshall, and Cooley 1997). It can evolve
to become the standard method of choice only if selection continues for a long
time in one direction and the best choices continue to be beyond the previous
expressions of the trait. Thus, if females that choose extreme males outreproduce
those that do not, the choosing of extremes will spread. So will extremeness in
males; otherwise the females choosing them would not gain. Spreading or fixing
the choosing of extremes will inject a certain degree of inertia into the process.
For this reason, once an “extreme-choosing” tendency is in place, extremes in the
traits of the chosen individuals can pass beyond the form in which they are adap-
tive in any other sense and indeed can become disadvantageous in other contexts.
Some such conflict actually exists among all the compromises of selection on dif-
ferent traits of the organism because the effect of selection can only be enhance-
ment of the reproductive integrity of the organism as a whole rather than the state
of any of its individual traits. When selection is social, however—when it is a mat-
ter of individuals choosing other individuals in a mutualistic or reciprocal social
interaction rather than, say, competition to detect or capture food, or to escape
enemies more effectively—overshoots in adaptiveness in other respects, because
of choosing extremeness, will be more prominent.
The second special feature of Fisher’s runaway sexual selection is the feedback
resulting from the genetic partnership between males and females in jointly pro-
duced offspring. Trivers (1972, 166) described it as follows:
[I]f there is a tendency for females to sample the male distribution and to
prefer one extreme (for example, the more brightly colored males), then
selection will move the male distribution toward the favoured extreme.
After a one generation lag, the distribution of female preferences will also
move toward a greater percentage of females with extreme desires, because
the granddaughters of females preferring the favoured extreme will be
more numerous than the granddaughters of females favoring other male
444 { Human Social Evolution

attributes. Until countervailing selection intervenes, this female preference

will, as first pointed out by Fisher (1958), move both male attributes and
female preferences with increasing rapidity in the same direction.
We can note, first, that some aspects of human evolution that intrigue us, such
as brain functions that result in cleverness in social interactions, including sce-
nario building and testing the social future by weighing alternatives internally,
could have evolved partly through sexual selection. In view of the tendency of the
human brain to become larger across history, and of human behavior to become
more complex—and seemingly ever more rapidly after these features had exceeded
their counterparts in other species—we might be concerned to examine the like-
lihood that runaway sexual selection is involved. A related question is whether
some or all features of runaway selection can also occur in nonsexual social inter-
actions such as the high-risk forms of social reciprocity that are prominent only
in the human species.
At first one may imagine that there are no parallels in social selection allow-
ing it to become runaway. But the way an individual gains by selecting its social
partners parallels the ways an individual can gain from cooperative interactions
with a mate and from a mate’s parental care. In both cases there is likely to be
genetic change in both the ability to choose good partners and the background of
the favored phenotypic attributes because a mutually beneficial interaction can be
maintained only if, on average, both interactants gain.
Sexual selection is a distinctive kind of runaway selection because joint pro-
duction of offspring by the interacting pair causes the process to accelerate (see
Trivers quote above). The defining feature of runaway selection is not acceleration,
however, but the tendency of the process to go significantly beyond adaptiveness
in all contexts except within the particular selective race—much further beyond
adaptiveness in other contexts than is ordinarily the case in the myriad compro-
mises among the conflicting adaptive traits that create and maintain the unified
organism.
This aspect of runaway selection may hold for reciprocity selection, in which,
unlike in sexual selection, both parties can carry tendencies not only to choose
extremes but also to display extremes. In social selection, again unlike in sexual
selection (except in simultaneous hermaphrodites), an individual can play both
roles, of chooser and chosen, with respect to the same traits, and alternations of
roles can occur during extended interactions between particular partners. To the
extent that social success in ecologically dominant humans (see earlier) becomes
the central determinant of reproductive success, runaway reciprocity selection
may be a more viable possibility than Fisherian runaway sexual selection.
Fisherian runaway sexual selection presumably begins with a likelihood of heri-
tability (i.e., genetic variability) in both variations in choices and variations in cho-
sen traits. It is easy to see that in this circumstance such competitions, or races, will
lead to genetic changes, at first changing both the ability and tendency to choose
 Evolution and the Arts } 445

extremes and the nature of the extremes available for choice. Continuing mutations
and genetic recombination (outbreeding among temporarily isolated groups) will
tend to offer the choosing parties increasingly extreme possible choices, though
to a reduced degree as selection continues to remove heritable variations in trait
expressions and the trait becomes sufficiently maladaptive in contexts other than
sexual selection. From earlier arguments it is not easy to understand the extent to
which relevant heritability is likely to disappear, or even become trivial.
Diminution (or disappearance) of heritability in variations will not necessar-
ily change the tendency to choose extremes: in effect, if an ability and tendency
to choose extremes in any of a variety of social races (at least in humans) could
become genetically fixed in the population (including the ability and tendency to
learn from others, or from observation, the values of such choosing), it could still
offer advantages to the chooser of extremes (without evolutionary change in the
trait per se) because of the usefulness of even nonheritable trait variations chosen
in a social partner. Of course, there may be further evolutionary improvements
in the ability to identify and use extreme traits even after all choosers are already
choosing extremes.
On the other hand, heritable variations in what is chosen will result in a contin-
ued march toward greater extremes because this relative quality will not be fixed
in the way the ability to identify and favor extremes can be fixed; extremes can
be identified only by comparing whatever is available. In Fisher’s version of run-
away selection, extremes win reproductively at first because they are ecologically
superior, meaning functionally superior outside the choice situation itself. Later
they continue to win because they are sexually (or, here, socially) superior, even
though, as a result of the progress of selection involving choice of extremes, they
may have become so extreme as to be otherwise functionally (ecologically) infe-
rior. Here, “sexually or socially superior” means that the choosing parties will have
acquired a genetic composition that will cause them to choose the extreme, the
resulting choice of the extreme individuals itself causing the chosen individuals
to outreproduce.
Extremes, however, will be chosen whether or not, as extremes, they rep-
resent heritable variants. If extreme social performances yield special social
opportunities to those displaying them (e.g., via their reputations as achievers or
winners), then regardless of the basis for the superior performances (i.e., genetic
variant or not), winning performances can yield benefits to the kin or other
social associates of the individual with the extreme traits. Thus merely joining
social competitions or races can pay, though only heritable variations, includ-
ing the (variant) ability to choose the best from among multiple available races
that might be entered, will yield evolutionary change. Heritable variations in the
ability to choose appropriate races—including not only those generally likely to
be profitable but those in which the choosing individual, because of his or her
special traits, has a special likelihood of competing successfully—may be all that
is needed to drive runaway reciprocity selection. The more different ways that
446 { Human Social Evolution

success can be achieved through reciprocity competition, the more robust will
be this type of social selection. This is a kind of selection that will yield at least
part of the human type of social intelligence, perceptiveness, and perseverance.
As we all know, status (or “reputation”) can exist independent of the adoption of
a particular extreme in behavior, so the importance of any behavioral extreme
in changing some aspect of culture can also depend on whether a prestigious
person adopts, favors, or approves of it.
Since Fisherian runaway sexual selection in nonhuman organisms has
remained controversial (or theoretical), but social parallels to it may be robust in
human society, one may wonder if Fisher actually derived his idea from observ-
ing human social situations rather than from thinking about sexual selection
in the birds he ultimately used as his examples. If so, it is likely not the only
instance in which an evolutionist was inspired by human traits and tendencies
to develop a general evolutionary explanation (e.g., Darwin’s observations on
human selection of variations in domestic animals and the fact that Hamilton’s
rule applies in its fullest extent as extensive differential nepotism across multiple
levels of relatedness only in humans). This suggestion is ironic in another way,
in view of the success with which academic biology departments have managed
to exclude the human species from their consideration, leaving its analysis to
the almost exclusively nonevolutionary approaches of social science and medical
departments, and surely delaying acceptable explanations of the human species
in evolutionary terms.
When extremes in particular directions are being chosen in social selection,
new extremes never before experienced may be chosen above all other expres-
sions of a trait. This behavior was originally referred to in European ethology as a
“superoptimal stimulus” effect and is not specifically related to runaway selection.
Whenever superoptimal stimulus effects can be identified, however, they suggest
a history of choosing extremes, therefore the possibility of some form of runaway
selection. If, for example, we perceive that during the past several centuries art—or
even human sociality in general—has flourished and become an enormous and
diverse enterprise compared to any “ancestral” condition it might have exhibited,
we might suspect that this is evidence of a history of choosing extremes continu-
ally in short supply and consequently of some kind of runaway process in however
artistry affects the securing of the resources of reproduction. Rather than evidence
that evolution cannot be used to explain, say, the arts, explanations of recent flow-
erings of diversity and complexity in human enterprises can be sought by expand-
ing our understanding of the various subprocesses of evolutionary selection. We
should not be discouraged because the pathways to explanation become progres-
sively more difficult and call for expansions of our understanding of the workings
of the evolutionary process.
 Evolution and the Arts } 447

The Arts And Competition

Competitive races among humans, which include performances in the arts, can
take either of two directions. They can change in the direction that enables indi-
viduals to give performances that are unique, not easily compared to those of oth-
ers, and highly informative to observers about relatively complicated aspects of
sociality. These are the races that we would most often term “artistic.” Their par-
ticipants are likely to have carved out special life niches for themselves. In effect, a
flourishing of the arts in its most diverse forms reduces direct and confrontational
competitive races because it is more difficult to compare creative artists than to
compare, say, athletes in the same sports, chess players who contest one on one, or
people who try to best one another’s record in any uncomplicated or highly pat-
terned and predictable game or contest.
Trends toward individuality in performance and meaning in the arts—as in
poetry—can continue, paradoxically, because the value of gaining insight from the
brilliance of others is so great to us. The more profound an insight, as well as the
more personal or specific, the more difficult it is likely to be to absorb. This is the
reason that a poem can be so personal as to be understandable only to its author, yet
the author can be accorded high status because of the poem. Because they expand
and enhance our imaginations, poetry and art press continually at the boundaries
of mystery and incomprehensibility, so that, as audience, we are always faced with
the necessity of deciding whether the artist is incomprehensible because of tell-
ing us something unusually profound or because of telling us something trivial or
wrong in an obscure way. It is a difficult decision because we know in our souls that
the scoffer can lose as profoundly as the gull, whether the poetic message is used or
rejected directly or attempts are made to use it indirectly during social interactions
with the poet in some other context. The same challenge exists in the assessment
and use of humor as insight into the social scene, as all those who have laughed too
soon on at least one occasion will understand (Alexander 1986, 1989).
Socially competitive races that parallel those involved in the arts can also take a
different form, changing instead in directions that progressively narrow the varia-
tions available to the performers and the nature of the prizes and diminish the
social messages available to observers. Competitors in such races are forced into
increasingly or more directly confrontational races.
Modern humans have generated almost endless possibilities of being “world
class” in direct competitions, from championships in golf or boxing to first prize
in poetry or painting or musical contests to making the largest pizza or longest hot
dog in the world, flagpole sitting for the longest time, or establishing the fastest
construction times for field latrines in the history of the military. When reputation
comes to be based so strongly on relative achievement compared to other humans
that the nature of the competition becomes trivial and the relative ranking of the
448 { Human Social Evolution

competitor becomes paramount, extremeness in the competition may be repre-

sented by activities or “traits” so radical that, in all regards except the specific com-
petition being considered, they are disadvantageous to the individual exhibiting
them. Social messages for audiences, moreover, can be restricted to the identity
of contestants that finished in particular rankings. Nevertheless, such rankings
represent changes in social status or maintenance of social status.
I can give an example from horse competitions. Judged horse competitions are
like other judged contests: they can reach maddening levels of faddishness. These
endlessly competitive races involve a wide variety of things, including the details
of the clothing worn during different competitive classes; precisely how a rider
holds hands, feet, and head; minute details of the equipment worn by the horse;
and exactly how the horse holds its head. To take only one example here, in cer-
tain breeds, in a competition called “Western Pleasure,” a tendency arose to favor
horses that moved with their heads held somewhat lower than one is likely to see
on the random horse galloping across the prairie or walking in someone’s pasture.
This favoring evidently began because it was undesirable for horses used in ranch
work to hold their heads high enough to be in the way of the rancher’s work. But
lowered heads became a trend that reached such extremes that horses in these
Western Pleasure competitions came to be called “peanut rollers” because their
heads were so low they were jokingly regarded as able to roll peanuts as they walked
or jogged along. Meantime, in breeds originally bred to move elegantly in parades
and the like, and in others to show off unusual gaits, precisely opposite trends
were set in motion in similar competitive classes. The horses were encouraged or
forced to hold their heads higher and higher until the neck was essentially vertical.
While some horse people were drugging their horses, starving them, or bleeding
them (yes, I do mean those things) to get their horses to keep their heads down
and move ever more slowly (and dejectedly!), those working with other breeds
were letting their horses’ fore hooves grow long so as to lift their front ends and
their heads even higher. Eventually some of the latter people began placing plastic
and other kinds of extensions on their horses’ front hooves so that they appeared
to be walking with their forefeet on boxes. And the riders began to sit farther and
farther to the rear on the horse’s back so that the horse would have a greater ten-
dency to lift its front end in a fancy way while traveling around the show ring. This
position became so extreme that riders began to wear capes that flowed over the
horse’s rump and to place bulky garlands across the saddle in front of them, both
items evidently to conceal how embarrassingly far back the rider was sitting on the
horse. Finally, some of the people with a certain breed of horses began to “sore” the
tender portions of their horses’ forefeet with acid or a knife, and to train the horses
with heavy bruising chains around the tops of their hooves, in both instances so
that they would lift their feet (and their heads) even higher. It seems sometimes
that no judged contest of humans can maintain a happy medium in any one trait or
action or fail to become narrow and faddish. Extremes appear, are quickly favored,
and eventually become so ridiculously exaggerated as to discourage many people
 Evolution and the Arts } 449

from participating. Perhaps only periodic dramatic changes in direction seriously

retard such extreme trends.
Extremes of judging in narrow competitions are not restricted to small audi-
ences or small-time events, as anyone knows who watches events such as figure
skating or gymnastics in the Olympic Games. But for individuals or teams rep-
resenting institutions (or nations), the social message has to do with competition
between the institutions, meaning that, because of their symbolism, even narrow
and confrontational races with little relationship to social questions or broadly
important qualities of the contestant can attract huge audiences and yield high
status for excellence in performance.
The incredible tendency of humans to engage in competitive races and carry
them to extremes tells us that such competitions must be a very old part of our
makeup, and a part that somehow furthered our reproduction. A point with which
such races are entirely compatible is that organisms do not evolve just to repro-
duce successfully but to outreproduce everyone like them.
Whenever tendencies exist to recognize and admire “winners,” whether they
are outstanding artists, musicians, actors, dancers, poets or writers, shamans,
humorists, athletes, war heroes, or thinkers, the tendencies may result in pro-
longed evolution, exaggerating the bases for the skills represented, perhaps pro-
ducing the extreme skills and capabilities exhibited in the arts today. To the extent
that such capacities tend to have a common genetic basis, the selection could be
even more effective. Thus a wide variety of artists might achieve their special abili-
ties partly through a common ability to construct and retain mental scenarios.
Whether or not the most talented and specialized artists could use their special
abilities to succeed in the social scene, their (genetically recombined) offspring
might have superior skills in a variety of social situations. The favoring of seem-
ingly different capabilities could have had common ground that led to the exag-
geration of rather specific mental capacities, to which we have given labels such
as “intelligence,” “genius,” or “perspicacity.” The prediction from this suggestion is
that people unusually capable in one intellectual or other endeavor in the arts are
likely to be unusually capable in others as well. To the extent that this generaliza-
tion is accurate, and tends to involve the useful skills of humans very broadly,
the concept of “maladaptive in other contexts” because of dramatic overshoot in
particular traits is diminished. While reciprocity selection is evidently distinctive
and influential in humans, the question of whether it involves a runaway process,
at least in the Fisherian sense, remains unclear.
In the 1930s and 1940s, the newsreels that preceded showing of movies in the-
aters proclaimed that in the twenty-first century people would not have to work
more than fifteen or twenty hours a week because technological devices such as
robots and calculating or computing machines would take care of most of the
mundane tasks humans had to do then. As a specific example, when the labor-
saving three-point hitch was developed for small farm tractors (in England by
Harry Ferguson), its glory was assumed to be that it would allow the small farmer
450 { Human Social Evolution

to do all the necessary work on his 160 or so acres with considerably less time
and effort, giving him extra leisure time. In both this special case and in general,
the virtual opposite has happened. Today in the United States, in many or most
families both parents work even more than one parent worked in the early part
of the twentieth century, and children are—seemingly “necessarily”—relegated to
day care and preschool. Farmers found that the three-point tractor hitch actually
helped set off a new competitive race that required farmers to multiply the num-
ber of acres worked in order to make a living wage. Instead of having more leisure
time, farmers were able to do more work in the same time, and, like everyone else
in the same situation, they seemed to be essentially forced to do that to keep up
with or forge ahead of everyone else. More recently, the advent of efficient hydrau-
lic systems on tractors has largely superseded the three-point hitch and set off a
new race in which a single family may find itself working one or two thousand
acres while selling such products as corn and other grain at prices not too different
from those paid when the three-point hitch was invented more than a half-century
ago. All of this speaks again to the fact that, like other organisms, humans must be
presumed to have evolved not merely to reproduce successfully but to outrepro-
duce their most significant competitors, leading to the proliferation of unending
competitive races.
As implied in the above discussion of so-called labor-saving devices, we can
perhaps be bold enough to ask whether concatenations of some human socially
competitive races, because of their combined diversity, narrowness, and runaway
and faddish effects, may even have value in comprehending why Barzun (2000)—
and others—have felt it necessary to interpret both long- and short-term trends in
human sociality as decadent.
Throughout the history of such narrow and frantic competitive races, some-
thing more properly called “art” has persisted, apparently because of a sec-
ond attitude toward competitive races (both strategies can be witnessed being
employed by children in that microcosm of the human social world that consists
of competing for the approval of a single set of parents). One expression of this
second attitude I have earlier described as avoidance of directness in competi-
tiveness rather than the seeking of ever-more confronting forms or expressions
of competition.
Another similar expression may arise, not through avoidance, but through the
incidental perception and adoption of new and appealing avenues of creativity.
Whatever their origin, unique life niches are created by some humans for them-
selves, from which they are able to tell the world things that no one has ever known
before. Perhaps, as individuals, these artists can indeed be said to have mounted
the “single-minded effort to render the highest kind of justice to the visible uni-
verse” alluded to by Joseph Conrad (quoted in Barzun 2000, 791). Incidentally,
they also magnify the social diversity that we humans euphemistically refer to as
“division of labor.”
 Evolution and the Arts } 451

CONCLUSION
In sum, I have tried to consider every relevant aspect of the topic I originally pro-
posed. At least I don’t think I left any gaps that might require miracles. If that is
true, perhaps this essay helps make it more likely that some day we will know how
to connect the entire array of human activities to a base in reproductive effort.
The undertaking is important because it promises dramatic insights into our
most precious thoughts and strivings, and those most stubbornly resistant to
change. Such human self-understanding may be the most important change imag-
inable in our universe, not merely to promote happiness and well-being but to
lengthen human lifetimes by reducing needless strife and aggression at all levels.
We think of the arts as differing from the sciences in seeking meanings—social
facts that are often restricted in their usefulness, or personal rather than general.
Part of the reason for the restrictions may be that the uniqueness of individual
human genomes has resulted in each of us evolving to behave (in evolutionary
terms, appropriately) as if, for each of us, the collection of our personal life inter-
ests were unique. We have evolved to use the myriad facts available to us in ways
unique to ourselves, which in some sense is the meaning of meaning. Human
social races are prevalent because of the importance of the prestige thought to be
derived from doing well in almost any such race and the consequences of prestige
that bring benefits (power) through the action of direct and indirect reciprocity.
Evolutionary social selection, including nepotistic selection and mutualistic and
reciprocity selection, may be the last important set of mechanisms required for the
connecting of complex aspects of cultural phenomena, such as the arts, to a life
basis in evolutionary selection favoring reproductive success. It leads to the exag-
geration of all the capabilities that are displayed in artistic works and performances.
I recognize that all of my discussions are imperfect and incomplete. They will
be worthwhile, however, if the shortcomings help point the way for those with the
next round of insights. I conclude that we seem not to be lacking in mechanisms
to approach analysis of our own activities in evolutionary terms, only in knowing
how to use them. Perhaps the next generation can make sense of the rudimentary
arguments that I and others have generated so far on these difficult topics.

NOTE
I am deeply indebted to four of my former students. Dr. Andrew F. Richards
has considered most of these issues with me across the past several years nd has
criticized the manuscript at several stages. Beverly Strassmann, David Marshall,
and Mary Jane West-Eberhard provided stimulating criticisms of the chapter
on short notice. David Lahti has also helped me immensely by consistently put-
ting forth useful and constructive arguments. Because I did not accept all of the
efforts to help me, I stress my own responsibility for any remaining errors or
awkwardness.
452 { Human Social Evolution

POSTSCRIPT
Epitaph

Who gains the privilege to pass,

With mind still undiminished,
Submits to this sad epitaph,
Alas! I was not finished.

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Alexander, R.D 1986. Ostracism and indirect reciprocity: The reproductive significance of
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Alexander, R.D 1987. The Biology of Moral Systems. Hawthorn, New York, Aldine de Gruyter,
xxii + 303 pp., 8 figs.
Alexander, R.D 1989. The evolution of the human psyche. In: C. Stringer and P. Mellars
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and B. J. Crespi, 4–31. Princeton, N.J.: Princeton University Press.
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Fisher, R. A. 1930 (1958). The Genetical Theory of Natural Selection. 2nd edition. (1958).
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Henrich, J. and F. J. Gil-White. 2001. The evolution of prestige. Freely conferred deference as
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Lessing, D. 1992. African Laughter: Four visits to Zimbabwe. New York: Harper.
Miller, G. F. 2000. The Mating Mind: How Sexual Choice has Shaped the Evolution of Human
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Sahlins, M. 1976. Culture and Practical Reason. Chicago: University of Chicago Press.
Trivers, R. L. 1971. The evolution of reciprocal altruism. Quarterly Review of Biology 46:35–57.
Trivers, R. L. 1972. Parental investment and sexual selection. In: B. Campbell (ed). Sexual
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Index

“About the Social Contract” (Alexander), 39 on altriciality, 8–9, 173–74, 176–77, 179,
Ache of Paraguay, 140 182–90
adaptation arts and, 13–14, 426–37, 440–51
comparative animal behavior and, 33, biography of, 1–4, 25–26
35–36 The Biology of Moral Systems by, 4–5,
defined, 250 40–41, 95, 199, 314
humor and, 337–42 The Biology of the Naked Mole-Rat by,
affiliative humor, 338, 345, 355 5, 56
African Laughter (Lessing), 413 “Bragging Rights” by, 123
aggression childhood and, 171, 173–79, 182–94
in On Aggression and The Territorial comparative animal behavior and, 26,
Imperative review, 2, 7, 125–28, 29–37
130–37 concealed ovulation and, 7–8, 139–48,
altruism and, 130–32, 134–37 152–67
balance of power and, 262 cooperation and, 39–46, 48–51, 364–71,
culture modifying, 133 375–77
early, 293 culture, biology and, 93–100, 96t,
evidence of, 294–96 104–20
family groups and, 134–35 Darwinism and Human Affairs by, 2–3,
genetics and, 125–26, 133 95, 139
group-coordination and, 288–89 ecological constraints and, 364–71,
hunting and, 133–36 375–77
natural selection and, 125–26, 131–33 error by, 71–73
in parental care, 135 on eusociality, 5, 12, 53, 55–59, 63–68
social structure and, 134–35 “Evolution and Human Behavior”
threats in, 132 course of, 3, 8
in warfare, 125–27, 133, 135–37, 293 “Evolutionary change in cricket acousti-
“Aggressiveness, territoriality, and cal communication” by, 25
sexual behavior in field crickets” evolution of intelligence and, 232–33,
(Alexander), 24 235–41, 244–97
agriculture, 128 “God, Most Recently” by, 379–80
AIDS, 260 “Heroes Are Works of Art” by, 53
Alexander, Richard D. humor and, 334–35, 337–42, 345–61
“About the Social Contract” by, 39 indirect reciprocity and, 197, 199–206,
On Aggression reviewed by, 2, 7, 125–28, 209–39, 210t–213t, 227f
130–37 insects and, 23–26, 23f
“Aggressiveness, territoriality, and sex- intergroup competition and, 14–15, 123,
ual behavior in field crickets” by, 24 125–28, 130–37, 155–56
454 { Index

Alexander, Richard D. (Cont.) genes and, 80, 326

kinship, parental care and, 138–48, genetic, 214, 216, 252–54, 319
152–67 indiscriminate, 227, 227f, 328–29, 332
legacy of, 3–15 net-cost, 393
“Life Effort” by, 70 in parental care, 135
morality and, 9–11, 199–206, 209, 215– as positive sociality, 393–94
30, 305, 307–22, 325–33 reciprocity and, 200–202, 205, 211t, 212,
on parent-offspring conflict and manip- 214–16, 220, 223–24, 226, 346
ulation, 70–75, 77–87 rewards and, 211t
“People! People!” by, 364 self-deception and, 314
“Phantasm” by, 21 androgens, 143
“Reality and the Human Enterprise” by, anti-Gods, 332
232–33 ants
religion and, 12–13, 379–421 army, 65
“Reverse Reciprocity” by, 197 food and, 370
“The Role of Behavioral Study in Cricket red fire, 307
Classification” by, 25 worker, 55
“To a Life Mate” by, 138 aphids, 375
within-group cooperation and, 14–15, aquatic mammals, 191
123, 125–28, 130–37 Arab world, 420–21
alloparenting arbitrariness, in culture, 117–20
in eusociality, 55 Ardrey, Robert, 2, 7, 125–28, 130–37
human, 59, 99, 176 army ants, 65
Hymenoptera, 73 arts
altriciality Alexander and, 13–14, 426–37, 440–51
Alexander on, 8–9, 173–74, 176–77, 179, audiences of, 440
182–90 cave painting, 430
of babies, 182–90, 192, 272 challenge of, 429
of birds, 182–83, 185–88, 191 competition in, 436–37, 447–50
in childhood, 8–9, 173–74, 176–77, 179, culture reflected by, 14
182–90 development of, 429–30
concealed ovulation and, 188 extremes in, 436–37, 443–45, 448–49
defined, 174, 182 human evolution and, 13–14, 426–37,
ectothermy and, 191 440–51
hairlessness and, 193–94 humor and, 340–41, 440
of insects, 183, 187, 190 importance of, 451
juveniles and, 184–90, 193–94, 278 inclusive fitness theory and, 432, 437
neoteny and, 176–77, 192 individuality in, 447
of nonhuman animals, 182–88, 191–94 language in, 440
parental care and, 176, 184, 189–90 meaning in, 451
altruism mind’s eye in, 430, 434
aggression and, 130–32, 134–37 morality and, 434–35
defined, 319 motivation in, 432
degrees of, 330–31 myth in, 414
discriminative, 328–29 natural selection and, 437
egoism and, 314 nonhuman animals and, 429
eusociality and, 56–57, 83–85 pleasure in, 431–32
 Index } 455

prehistoric, 430 diversity of, 29, 34–35

problem-solving in, 432 genetics and, 29, 34–37, 109, 275–80
reputation and, 434–35 human evolution and, 30–31, 110–11
scenario-building in, 433–34, 441 learned, 275–76
science and, 451 plasticity in, 36, 100
self-deception and, 432–33 rigidity of, 258
sexual selection of, 430–32 behavioral ecology, 126, 140
social/intellectual play in, 433–34 Benedict (saint), 368
social selection and, 429–37, 442–46, beneficence. See also indiscriminate
451 beneficence
social skills in, 440–41 in direct reciprocity, 224
status and, 434–35, 441–42, 446 discriminate, 224–30, 227f
as theater, 440–41 distinctive aspect of, 254
theory of, 340–41 eusociality and, 224
value of, 434 for later generations, 409
visualization in, 430, 434 in nepotism, 224
atoms, of sociality, 209–16, 210t–213t return, 394, 418
audiences, of art, 440 universal spirit of, 407
Augustus, 367 benefits. See costs and benefits
Australia biases, inherited, 436
Martu aborigines of, 140 Bierce, Ambrose, 356
movement to, 292 Bigelow, Robert S., 123, 401, 404
autocatalytic model, 245, 261–62, 291 biology. See also evolutionary biology
automatization, 281 culture and, 93–100, 96t, 104–20
autonomy, of humans, 433 education in, 408
Axelrod, Robert, 40, 199–200 of learning, 96–97
morality and, 309–11, 314, 325–33
babies sociobiology and, 109, 235
altriciality of, 182–90, 192, 272 The Biology of Moral Systems (Alexander),
doctors and, 218–19 4–5, 40–41, 95
smiling and laughing, 352 indirect reciprocity in, 199
baboons, 160, 163, 264 morality and, 314
balance of power The Biology of the Naked Mole-Rat
aggression and, 262 (Sherman, Jarvis, and Alexander),
between groups, 247–48, 258–62, 294, 5, 56
361 birds
importance of, 404 altriciality of, 182–83, 185–88, 191
intelligence and, 247, 258–62, 294 eusociality and, 67
intergroup competition and, 262, 294 song patterns of, 35
power races in, 247–48, 258–62, 294, Blackburn College, 1
361, 404 Blick, James, 72
bared-teeth grin, 338, 352 blind faith, 405
bees, 67, 79, 81, 85–86, 365–66. See also bonding
honeybees humor and, 337–39, 345
behavior. See also comparative animal pair, 140–41
behavior; selfish behavior bonnet macaques, 157
courtship, 35–37 Borror, Donald, 23–24
456 { Index

“Bragging Rights” (Alexander), 123 intelligence and, 239–40, 253, 256, 263–
brain 64, 288, 293
cultural, evolution of, 98–99 laughing, 341, 351
dolphin, 293–94 semen of, 147–48
learning collected in, 399 social organization of, 160–61, 263, 293
size, 131, 134, 136, 184, 240, 291, 296– China
97, 404, 442 eunuchs in, 367, 371
in Social Brain Hypothesis, 237, 240–41 group size in, 51
breeding Christine of Ardres, 368
cooperative, 57–59 church, 1
inbreeding, 127, 134 civilization, beginning of, 370–71
classical theory, of social evolution, 40
Cabot, John, 371 climatic instability, 240, 297
Caesar, 367 clones, 257
Callahan, D., 217–18 Clovis, 368
canines coalitions, 257
play in minds of, 271 cognition, 273–74
sociality in, 256–57 cognitive psychology, 267
cannibalism, 132, 136 collateral relatives, reproduction via,
Carneiro, Robert, 371 377–78
caterpillars, 376–77 collective, mind of, 409–10
cave painting, 430 Columbus, Christopher, 371
celibacy, 366, 369–70 communication
cellular competition, 43–44 cricket, 25, 34
Charlemagne, 368 displacement in, 290
Charles I, 369 with emotion, 285–87
cheating, 212t humor and, 351
childhood comparative animal behavior
Alexander and, 171, 173–79, 182–94 adaptation and, 33, 35–36
altriciality in, 8–9, 173–74, 176–77, 179, Alexander, 26, 29–37
182–90 instinct and, 33–37
neoteny and, 176–78 method of, 31–32, 37
pleiotropy and, 174–78 systematics and, 26, 29–37
senescence theory and, 175, 177–79 comparative method, 31
children competition. See also intergroup
caring for elderly parents, 217–18 competition
culture and, 96, 99 in arts, 436–37, 447–50
hairlessness of, 174–78, 192 cellular, 43–44
precociality and, 174–76, 182–88 chimpanzees and, 239–40
chimpanzees cooperation and, 14–15, 254, 259–61,
attributes of, 153, 157, 263 266
competition and, 239–40 culture and, 98, 155, 262
displacement and, 290 directions of, 447
group selection and, 253 extended social networks and, 241
hunting by, 256 father-mother, 85–86
indirect reciprocity and, 214 in games, 403
 Index } 457

group, 43, 155, 204–6, 258–62 parent-offspring conflict and

horse, 448 manipulation
humor and, 271–72 between God and evolution, 411–14
hyper-competitiveness, 414, 416 group living and, 390–93
intelligence and, 254 kin, 2
intensification, 155–56 local hubris, 413
internal, 41–46 conflicts of interest
intra-ejaculate, of sperm, 44–45 among babies, doctors, and parents,
intraspecific, 30, 132 218–19
male-male, 431 defined, 220
morality and, 312–13 elder care and, 217–18
nastiness of, 266 eusociality and, 327
religion and, 398–99, 402–4, 411 genetic differences causing, 327–28
reproduction and, 132, 254 group selection and, 251–52, 258
reputation and, 447–48 importance of, 346
runaway social, 247–48, 258–62, 294 indirect reciprocity and, 216–21
sexual, 158, 431 morality and, 216–21, 325, 327–29
suppression of, 41–46, 204 ostracism and, 346
team, in sports, 402–4 about parental care, 71–72
warfare and, 239 runaway social competition and, 260
concealed ovulation confluences of interest, 253, 329, 346
Alexander and, 7–8, 139–48, 152–67 conformity, 100
altriciality and, 188 congeniality, cooperation and, 266
Dogon of Mali and, 139, 142, 144–48 Conrad, Joseph, 450
EPC and, 145–47 conscience
evidence for, 139–48 consequences and, 274
female orgasm and, 164–65 injustice and, 305
hairlessness and, 165 as override, 346
hormones and, 142–43 consciousness
human evolution and, 152–67 as distinctive human attribute, 153, 155
morality and, 307 evolutionary determinism and, 278–80
ovulation cues and, 141–44 inner eye of, 288
parental care and, 7–8, 140–41, 145–46, motivations and, 432
152–67 muting of, 394–99, 415
paternal care and, 140–41, 145, 152, observation and, 272
156–58, 160–61, 164 as override, 346
precociality and, 188 psyche and, 244, 267
purpose of, 157–63 purpose and, 406–7
rape and, 163–64 selflessness and, 418
selection and, 141–42, 157–58 sociality and, 267
self-awareness and, 166–67 system of, 235–36, 267
self-deception and, 166–67, 282–83 Constantinople, 367
social evolution and, 152–67 Continental Congress, 371
upright locomotion and, 165–66 continuous sexual receptivity, 157–58, 163
concealment, 282–83 cooperation. See also within-group
conflict. See also intergroup conflict; cooperation
458 { Index

cooperation. (Cont.) art reflecting, 14

Alexander and, 39–46, 48–51, 364–71, biology and, 93–100, 96t, 104–20
375–77 changes in, 112–17
competition and, 14–15, 254, 259–61, children and, 96, 99
266 competition and, 98, 155, 262
congeniality and, 266 in Darwinism and Human Affairs, 95
ecological constraints and, 364–71, defined, 111
375–77 as distinctive human attribute, 153,
evolution of, 4–5, 13–15, 40, 237 155
humor and, 355–56 dynamic, 100
individual costs and benefits driving, evoked, 97
125 genetics and, 113–16, 119–20, 434, 436
among insects, 45–46, 49–50 heritability in, 114–16, 119
kinship mitigating, 370 human evolution of, 6–7, 93–100, 96t,
monogamy and, 43, 49–51 104–20
morality and, 318 indirect reciprocity and, 222
new theory of, 40–46 as key setting, 434
peer-punishment promoting, 204 learning and, 109–11, 117, 442
religion enhancing, 13, 237–38, 382, Malinowski and, 115, 118–19
398, 411, 419 Murdock and, 96, 96t, 113
reproductive opportunity leveling and, natural selection and, 98, 104–17, 120
48–49 novelty and, 97, 99–100
reproductive success and, 355 social selection contributing to, 97–98,
special cases of, 48–50 442–46
Tit for Tat and, 201–2 theory, 111–19
cooperative breeding, 57–59 transmission of, 436, 442
Cornell University, 56, 144–45 utilitarianism and, 112
costs and benefits
environmental, 280 dance language, of honeybees, 290
individual, cooperation driven by, 125 Darwin, Charles, 190, 271
ratio of, 202, 215, 253, 280 challenge of, 386
courtship behavior, 35–37 Descent of Man by, 200, 370
cousin marriage, 127 divinity taken up by, 369
cowboy movies, 402 empathy and, 321
coyness, 35–37 genes and, 386
creationism, 104–5, 127 hostile forces of nature of, 248, 296–97
creativity, 247–48, 268, 450 on laughter, 338, 352
crickets methods of, 349
altriciality of, 183 natural selection and, 104–5, 259, 365,
communication of, 25, 34 386, 429
field, singing male, 23, 23f On the Origin of Species by Means of
taxonomy of, 23–26, 23f Natural Selection by, 365, 386
cultural brain, evolution of, 98–99 reciprocity and, 200, 205
culture religion and, 385–86
aggressiveness modified by, 133 sterility and, 77–78, 365–71, 375–77
arbitrariness in, 117–20 Wittgenstein on, 309
 Index } 459

Darwinism displacement, in communication, 290

cricket taxonomy and, 23–26, 23f distrust, 223
social, 310 divinity
Darwinism and Human Affairs (Alexander) Darwin taking up, 369
culture in, 95 natural selection and, 104–5
watershed moment of, 2–3, 139 division of labor
David, 366–67 creativity and, 450
Dawkins, Richard, 200, 235, 416, 432 reproductive, 59, 366
death doctors, conflicts of interest with, 218–19
deterioration leading to, 408 Dogon of Mali
of males, 393 features of, 145
from violence, 400–401, 404 fieldwork among, 139, 145
deception. See also self-deception menstrual cycle in, 139, 142, 144–48
ability, 166–67 dolphins, 293–94
emotion and, 286 domain-specific modularity, 99–100
indirect reciprocity and, 212t drift, 115, 250
intelligence and, 249, 274, 281–84 drive suppression, 42
intergroup conflict and, 283–84 duality, in human nature, 326, 396
sincerity and, 281 dual mating strategy, 145–48
subconscious and, 282–83 Durkheim, Emile, 381
tactical, 236–37
Declaration of Independence, 371 early aggression, 293
deliberateness, 273 early group living, 388–89
democracy, 369 ecological constraints
Descent of Man (Darwin), 200, 370 Alexander and, 364–71, 375–77
despotism, 289–90 cooperation and, 364–71, 375–77
determinism, 109, 275, 278–80, 333 on eusociality, 6, 11–12, 370–72
Detroit, 400 sterility and, 365–71
Devils, 332 ecological dominance, of humans, 247–48,
differential nepotism, 441–42 291, 417
diploid male termites, 80 economics, 205–6
direct nepotism, 210t, 212, 214, 216 ectothermy, 191–93
direct reciprocity education, in biology, 408
beneficence in, 224 Ego, assistance to, 211
God and, 420 egoism
human effort of, 210t, 214 altruism and, 314
indirect reciprocity compared with, evolutionary biology and, 311
199–204, 221 indirect reciprocity and, 209, 211–12,
investment in, 211 214
morality and, 327, 434–35 utilitarianism and, 10–11, 326
reasons for, 442 Egypt, 420–21
direct somatic effort, 209, 210t, 211, 215 elderly parents, 217–18
discriminate beneficence, 224–30, 227f Elkin, Stanley, 397
discriminating strategy, 202 emotions
discriminative altruism, 328–29 aspects of, 284
discriminative reciprocity, 328–29 changed, 285–86
460 { Index

emotions (Cont.) kinship and, 6, 57, 59

communication with, 285–87 in naked mole-rats, 5, 12, 53, 55–59,
deception and, 286 63–68, 366, 375
expression of, 284–90 natural selection and, 55
feelings and, 284–87 parental manipulation and, 73, 77–87
God and, 412 relatives in, 257–58
group-coordination and, 288–90 safe nests and, 57, 63–67
in human evolution, 284–88 seasonality influencing, 66
intelligence and, 238, 244, 274, 284–90 size influencing, 65–66
in warfare, 289 underground, 63, 65
empathy, 321, 350 vertebrate, 65–68, 365–66
endorphins, 238 evil, greatest, 381
environmental costs and benefits, 280 evoked culture, 97
EPC. See extra pair copulation evolution. See also human evolution; social
EPP. See extra pair paternity evolution
equity theory, 325–26 of cooperation, 4–5, 13–15, 40, 237
estradiol, 143 of eusociality, 5–6, 11–12, 55–59, 63–68,
estrogens, 143 375–77
estrone, 143 genetic determinism and, 109
estrus God in conflict with, 411–14
humans and, 141–44, 157 inclusive fitness theory and, 2, 119–20,
pseudo-, 157 179, 220, 275–76, 279–80, 376–77,
sham, 162–63 381, 397, 432, 437
eternity, 412 of laughter, 352
ethical nihilism, 316 macroevolution, 96, 105
ethnic markers, 237 microevolution, 96, 105
eunuchs, 366–67, 371 misconceptions about, 95–96
eusociality Murdock and, 96, 96t, 113
Alexander on, 5, 12, 53, 55–59, 63–68 natural selection as guiding force of,
alloparenting in, 55 108, 249
altruism and, 56–57, 83–85 of parent-offspring conflict and manipu-
in aphids, 375 lation, 70–75, 77–87
beneficence and, 224 pattern changes in, 106–7
birds and, 67 people caring about, 265–66, 385–86,
characteristics of, 55 395
conditions leading to, 64, 83 philosophy and, 308–16
conflicts of interest and, 327 rapid, 245
cooperative breeding and, 57–58 science, recentness of, 385–89
defined, 55, 59, 375 based on selfish behavior, 416
ecological constraints on, 6, 11–12, speciation in, 106–7
370–72 of sterility, 12, 77–80, 83–84, 86–87
evolution of, 5–6, 11–12, 55–59, 63–68, systematics and, 24
375–77 “Evolution and Human Behavior” course,
food and, 370 3, 8
in Hymenoptera, 55, 63, 67, 73, 78, evolutionarily stable decision rule, 59
80–81, 375 evolutionary biology, 199, 385, 411
in insects, 55–57, 65–66, 77–87 egoism and, 311
 Index } 461

morality and, 309–11, 332–33 free will, 273, 320

questions of, 1 Freud, Sigmund, 288, 347, 350–51
“Evolutionary change in cricket acoustical frustration, 347–48
communication” (Alexander), 25 Frye, Billy E., 394–95
evolutionary determinism, 275–80 full-cost play, 281
extended social networks, competition functional theory, of culture, 118–19
and, 241
extra pair copulation (EPC), 145–47 gallows humor, 347
extra pair paternity (EPP), 145–47 games
extraparental effort, 210t competition in, 403
extremes repeated, 206
in arts, 436–37, 443–45, 448–49 theory of, 321
heritability and, 444–45 generalized reciprocity, 346. See also
in risk-taking, 284 indirect reciprocity
status and, 446 general theory of interest, 217
tendency to choose, 436–37, 443–45 genes
for altruism, 80, 326
fair meiosis, 42–43, 45 culture coevolving with, 434, 436
faith, 404–5 Darwin and, 386
family in good genes hypothesis, 431
groups, aggression and, 134–35 morality and, 312–13
method, of selection, 376 opportunity leveling and, 48–49
within-group cooperation in, 134 outlaw, 307
fantasizing, 274–75 replication of, 96
fathers, 85–86. See also paternal care genetic altruism, 214, 216, 252–54, 319
feelings, 284–87 genetic determinism, 109, 275, 333
felines, sociality in, 256–57 genetic fallacy, 310–11
females. See also women genetics
courtship of, 35–37 aggression and, 125–26, 133
dispersal of, 264 behavior and, 29, 34–37, 109, 275–80
orgasm of, 164–65 conflicts of interest and, 327–28
Feynman, Richard, 405 culture and, 113–16, 119–20, 434, 436
fish, 317–18 genetic variation
Fisher, Ronald A., 385, 443 learning and, 109–11
fly larvae, 187 natural selection and, 107–11
folk theorem, on repeated games, 206 traits and, 109–11
food Genghis Khan, 368
ants and, 370 genocides, 400–404
eusociality and, 370 genomes
stress, 292–93 opportunity leveling and, 48–49
foraging innovations, 240 origin of, 41
foresight, 153, 155, 267, 273, 346 germ-soma separation, 43–44, 175
fortress defense, by naked mole-rat, 57, gibbons, 157, 159
63–66 glaciation, 297
fossil evidence, 29, 31, 296 global harmony
Fox, William, 369 intergroup competition and, 417
freeriders, 204, 237–38, 393 nations in, 414
462 { Index

global harmony (Cont.) predation and, 255–56, 264, 288

positive sociality and, 393–94 reasons for, 236, 254–58, 264, 389–94
religion and, 379–421 reciprocity and, 442
self-understanding and, 408, 415, 418, religion and, 382, 388–94
420, 437, 451 sociality and, 255
solutions for, 414–21 groups. See also group living; group
team sports promoting, 403 selection; intergroup competition;
warfare and, 385, 390–94, 414–19 intergroup conflict; within-group
God cooperation
alternative explanations of, 387–88 balance between, 247–48, 258–62, 294,
anti-Gods and, 332 361
concept of, 331–32, 381–89, 395, 397– bonding in, 337–39, 345
99, 408–13, 417–20 causes of, 256–58
direct reciprocity and, 420 cohesion in, 41
emotions and, 412 competition and, 43, 155, 204–6, 258–62
evolution in conflict with, 411–14 coordination, emotions and, 288–90
indirect reciprocity and, 420 diverse, 390
kin and, 13, 420 expansion of, 392
meaning of life and, 406–7 family, aggression and, 134–35
as metaphor for unity, 381–83, 410, 418 hunting in, 255–57, 264, 288–89
morality and, 408–11 ingroup/outgroup hypothesis and,
in phrases, 410 337–39
realness of, 411–12 integrated, 44
universality of, 408–11, 419 mystery of, 396
“God, Most Recently” (Alexander), 379–80 political, 258, 291
good genes hypothesis, 431 size of, 41, 51, 58–59, 67, 127, 162, 238–
goodness, 314–17 41, 245, 262
Good Samaritan, 226 group selection
goosey, 351 chimpanzees and, 253
gorillas, 147, 157, 160, 239–40, 341 conflicts of interest and, 251–52, 258
grandchild effects, 411, 413 intelligence and, 251–54, 258, 266
great apes intergroup competition and, 205
mental attributes of, 293 loose thinking, 71
socioecology models of, 239–40 warfare and, 205
greatest evil, 381
“great man” theories, 118 HADD. See hyperactive agency detection
Greece, 367 device
Green, Ben K., 358 hairlessness
green beard, 307 altriciality and, 193–94
Gregory, 368 of children, 174–78, 192
grin, 338, 352 concealed ovulation and, 165
grooming, 353–54 ectothermy and, 191–93
group living hormones and, 176, 178
conflict and, 390–93 hunting and, 190
early, 388–89 in late juvenile and adult humans,
intelligence and, 236, 254–58 190–94
kinds of, 391 mammalian variations in, 191–94
 Index } 463

of naked mole-rat, 191–93 concealed ovulation and, 152–67

paternal care and, 165 of culture, 6–7, 93–100, 96t, 104–20
Haldane, Helen Spurway, 377 early stages of, 288–89
Hale, Nathan, 407 of emotions, 284–88
Hamilton, William humor in, 12, 222, 334–35, 337–42,
influence of, 2, 40, 56, 71, 73, 77–78, 345–61
85–86, 199, 377 indirect reciprocity and, 226–27
reciprocity and, 199–200 initial kicks of, 262–65
Hamilton’s Rule, 57, 59, 75 morality and, 9–11, 305, 307–22, 325–33
Handicap Principle, 272, 430–31, 436 natural selection and, 105–11, 254
haplodiploidy, 56–57, 73–74, 81 nonhuman animals and, 4
harmony. See global harmony novelty influencing, 97, 99–100
Heath, Noble Porter, II, 23 process of, 114–15
heaven, 408 of psyche, 9–10, 267–90
helplessness. See altriciality religion and, 12–13, 379–421
Henry VII, 371 rules for writing about, 173
heritability three major puzzles of, 131, 136
in culture, 114–16, 119 warfare influencing, 291, 294–96
extreme choices and, 444–45 human psyche. See psyche
hero humans. See also childhood; human
ideal moral condition of, 330 evolution
prestige of, 253–54, 377 alloparenting by, 59, 99, 176
“Heroes Are Works of Art” (Alexander), 53 autonomy of, 433
Herriott, James, 357–58 babies, altriciality of, 182–90, 192, 272
hidden motivation, 432–33 distinctive attributes of, 152–55, 245–46
hidden traits, 399 duality in, 326, 396
Hinde, Robert, 289 ecological dominance of, 247–48, 291,
homeothermy, 191, 193 417
honeybees effort of, classified, 209–16, 210t–213t
dance language of, 290 estrus and, 141–44, 157
queen, 81, 86 failures of, 400–404
soldier-workers, 67 as hostile forces of nature, 402–4
hormones hypocrisy of, 313–14, 316, 318–19, 360
concealed ovulation and, 142–43 juvenile, 184, 187, 190–94
hairlessness and, 176, 178 migration of, 292, 393, 430
horse competitions, 448 phenotypes of, 396
hostile forces of nature sterility and, 366–71
Darwin’s, 248, 296–97 tendency of, 321
humans as, 402–4 humor
houses of worship, 1, 398 adaptive significance of, 337–42
human evolution. See also intelligence, affiliative, 338, 345, 355
evolution of Alexander and, 334–35, 337–42, 345–61
of art, 13–14, 426–37, 440–51 arts and, 340–41, 440
behavior and, 30–31, 110–11 bonding through, 337–39, 345
church and, 1 communication and, 351
climatic instability influencing, 240, 297 competition and, 271–72
464 { Index

humor (Cont.) parent-offspring conflict and manipula-

cooperation and, 355–56 tion in, 73, 78, 80–81, 83–85
enjoyment of, 339–41 hyperactive agency detection device
function of, 347–49 (HADD), 381–82
gallows, 347 hyper-competitiveness, 414, 416
in human evolution, 12, 222, 334–35, hypocrisy
337–42, 345–61 of humans, 313–14, 316, 318–19, 360
insight from, 447 sincere, 360
intelligence and, 267–68, 271–75 Hyslop, Gordon, 411–13
jokes, 337–39, 342, 350, 353, 357–60
kinds of, 351 ideal, in morality, 322, 329–32
language and, 338 ignorance, veil of, 42
laughter in, 338, 341, 348–49, 351–55, Illinois Normal University, 1
357–60 immoral acts, outcomes of, 223–24
learning and, 267–68 inbreeding, 127, 134
mature, 353 inclusive fitness theory
nonostracizing, 355–57 arts and, 432, 437
ostracism and, 337–39, 341–42, 345–61 evolution and, 2, 119–20, 179, 220, 275–
as practice, 271 76, 279–80, 376–77, 381, 397, 432, 437
in reward system, 340–41 intelligence and, 275–76, 279–80
scenario-building enhanced by, 340, 360 religion and, 381, 397
self-deception and, 360 sterility and, 376–77
sense of, 340, 352–53 India
sex differences in, 353 eunuchs in, 367
slapstick, 338 group size in, 51
smiling associated with, 338, 351–53 indirect nepotism, 210t, 214, 216
stages of, 353–55 indirect reciprocity
status and, 337–39, 349–60 Alexander and, 197, 199–206, 209–39,
vicarious aspects of, 272 210t–213t, 227f
wit and, 350–51, 353 atoms of sociality and, 209–16,
“Humor” (Alexander), 334–35 210t–213t
humorist, 356 in The Biology of Moral Systems, 199
hunting chimpanzees and, 214
aggression and, 133–36 classification of human effort and, 209–
amount of time spent in, 441 16, 210t–213t
by chimpanzees, 256 conflicts of interest and, 216–21
in groups, 255–57, 264, 288–89 culture and, 222
hairlessness and, 190 deception and, 212t
in prehistoric art, 430 defined, 199, 214, 346–47
Hutchinson, G. Evelyn, 189 direct reciprocity compared with, 199–
Huxley, Aldous, 416 204, 221
Huxley, Thomas H., 391, 416 discriminate beneficence and, 224–30,
Hymenoptera 227f
alloparenting, 73–74 egoism and, 209, 211–12, 214
eusociality in, 55, 63, 67, 73, 78, 80–81, elder care and, 217–18
375 God and, 420
 Index } 465

group competition and, 204–6 instinct, 33–37

human evolution and, 226–27 institutions, 204
indirect somatic effort and, 211 intellect, 131, 189, 245, 293
indiscriminate beneficence and, 224–30, intellectual play. See social/intellectual play
227f intelligence, evolution of
mechanisms, 201–2 Alexander and, 232–33, 235–41, 244–97
morality and, 9, 199–206, 209, 215–30, analysis of, 244–45
313, 326–27, 331, 382, 434–35 balance of power and, 247, 258–62, 294
nepotism and, 214 chimpanzees and, 239–40, 253, 256,
among nonhuman animals, 202, 214–15 263–64, 288, 293
ostracism and, 345–61 competition and, 254
philosophy and, 216–21 deception and, 249, 274, 281–84
punishment and, 221, 331 difficulties in advancing, 265–66
reasons for, 442 dolphins and, 293–94
reputation and, 14, 202–4, 434–35 ecological dominance and, 247–48, 291
rules and, 212t, 223–24 emotion and, 238, 244, 274, 284–90
systems, moral systems as, 221–22, 228 evolutionary determinism and, 275–80
indirect somatic effort, 210t, 211–12, freeriders and, 237–38
215–16 group-coordination and, 288–90
indiscriminate altruism, 227, 227f, 328–29, group living and, 236, 254–58
332 group selection in, 251–54, 258, 266
indiscriminate beneficence humor and, 267–68, 271–75
encouraged, 225–26, 229 inclusive fitness theory and, 275–76,
indirect reciprocity and, 224–30, 227f 279–80
utilitarianism and, 225 intergroup competition and, 239, 283–
individual costs and benefits, cooperation 84, 288–89, 291–92, 294–95
driven by, 125 language and, 238, 244, 246, 248–49, 290
individuality, in arts, 447 Machiavellian Intelligence Theory of,
infanticide, 156 236–37
inference, strong, 141 natural selection and, 245–97
information processing, 97–99 nature of psyche and, 267–90
ingroup/outgroup hypothesis, 337–39 personality and, 244
inheritance, 114–16, 119 play and, 9–10, 236, 267–71, 274, 281
initial kicks, of human evolution, 262–65 problem-solving and, 246–47, 273–74
injustice, 305 representational ability and, 296
inner eye analogy, 288 runaway social competition and, 247–
insects. See also specific insects 48, 258–62
Alexander and, 23–26, 23f scenario-building and, 99, 248–49, 267,
altriciality in, 183, 187, 190 270–75
cooperation in, 45–46, 49–50 self-deception and, 249, 274, 281–84
eusociality in, 55–57, 65–66, 77–87 Social Brain Hypothesis of, 237, 240–41
monogamy in, 49 sociality and, 237, 240–41, 244–49, 255,
parental manipulation in, 72–73, 78, 281
80–85 testing of general hypothesis, 291–97
social evolution and, 21–37, 77–87 trigger for, 240, 262–65
sterility and, 12, 77–80, 83–84, 86–87 warfare and, 239, 246, 265
466 { Index

intent, 223, 273, 318 human, 184, 187, 190–94

intergroup competition late, hairlessness in, 190–94
Alexander and, 14–15, 123, 125–28, precociality and, 189
130–37, 155–56 reason for, 269
balance of power and, 262, 294
evidence of, 294–96 Keith, Arthur, 404
global harmony and, 417 Kelsen, Hans, 220
group selection and, 205 kin. See also relatives
importance of, 7, 155–56 cooperation and conflict, 2
intelligence and, 239, 283–84, 288–89, God and, 13, 420
291–92, 294–95 mysteries of, 396
population density and, 292 recognition, 228, 279, 328, 331
stages of, 295–96 selection, 46, 59, 73–74, 77–81, 83–85,
within-group cooperation and, 14–15, 236–37, 377, 420
123, 125–28, 130–37 kinship
intergroup conflict Alexander on, 138–48, 152–67
deception and, 283–84 cooperation mitigated by, 370
group-coordination and, 288–89 eternity and, 412
internal competition, suppression of, 41–46 eusociality and, 6, 57, 59
internet, reputation and, 206 parental care and, 138–48, 152–67
interspecies selection, 252 Kipling, Rudyard, 95, 95n1
intra-ejaculate competition, of sperm, Krugman, Paul, 420–21
44–45 Kublai Khan, 367–68
intraspecific competition, 30, 132
isolation, 115, 417 labor, division of, 59, 366, 450
Isoptera, 55. See also termite colonies labor-saving devices, 449–50
lactational amenorrhea, 145–46
James I, 371 language
Jameton, Andrew, 219 arbitrariness and, 117–18
Jansen, Albert, 219 in arts, 440
Jarvis, Jennifer, 5, 55–56 dance, of honeybees, 290
jokes group-coordination and, 290
best, 357 humor and, 338
in humor, 337–39, 342, 350, 353, 357–60 importance of, 99, 153, 238
kinds of, 357–60 intelligence and, 238, 244, 246, 248–49,
laughing at, 358–59 290
on sacred topics, 359 learning, 202
sex differences in, 353 reciprocity and, 202
telling, 358 scenario-building and, 290
tricks in, 338, 350, 358 shared myths and, 238
joking relationship, 354, 356–57 langurs, 157
justice, 307 late juvenile humans, hairlessness in,
“Just-so” stories, 95n1 190–94
juveniles laughter
altriciality and, 184–90, 193–94, 278 alone, 360
growth and development of, 185–86 in babies, 352
 Index } 467

in chimpanzees, 341, 351 males

Darwin on, 338, 352 competition between, 431
evolutionary origins of, 352 courtship of, 35–37
in humor, 338, 341, 348–49, 351–55, diploid, in termite colonies, 80
357–60 killed, 393
at jokes, 358–59 in multi-male primate bands, 160–62,
at someone, 350 239, 263, 293
from tickling, 351–52, 354–55 orgasm of, 165
too soon, 447 in single-male primate bands, 160
law, 332 Malinowski, Bronislaw, 115, 118–19
leaders, 386, 399 mammalian variations, in hairlessness,
learning 191–94
behavior, 275–76 manipulation, 6, 72–73, 286, 330–31. See
biology of, 96–97 also parent-offspring conflict and
collected in brain, 399 manipulation
culture and, 109–11, 117, 442 marriage, 127
by dolphins, 293 Martu aborigines, 140
forms of, 267 Masters, Roger, 348
genetic variation and, 109–11 mate guarding, 146–47
humor and, 267–68 mathematics, 246
kin recognition, 228, 328, 331 mating effort, 210t, 212
language, 202 mature humor, 353
in modern world, 413 meaning
morality, 202 arts seeking, 451
natural selection and, 109–11 concept of, 406
by observing, 268 of life, 387, 406–8
play and, 267–70 meiosis
Leigh, Egbert, 5, 42–43 fair, 42–43, 45
Lessing, Doris, 413, 441 reproductive opportunity leveling and,
LH. See luteinizing hormone 48–49
life, meaning of, 387, 406–8 memes, 119, 382
“Life Effort” (Alexander), 70 memory banks, accumulating and
Lincoln, Abraham, 414–15 modifying, 267, 272
local hubris, 413 Mendel, Gregor, 386
long-lived trees, 82–83 Mendelian segregation, 42–43
loose group selection thinking, 71 menopause, 152
Lorenz, Konrad, 2, 7, 125–28, 130–37 menstrual cycle. See also concealed
Louis XVI, 369 ovulation
luteinizing hormone (LH), 142–43 in Dogon of Mali, 139, 142, 144–48
Luther, Martin, 369 lactational amenorrhea and, 145–46
Lyell, Charles, 365 ovulation and, 142
sexual response during, 144, 148
macaques, 157, 160, 184 taboos, 145–46
Machiavellian Intelligence Theory, 236–37 mental precociality, 8–9, 174, 179, 272
macroevolution, 96, 105 mental prowess, 222
maggots, 187 metabolic rate, ectothermy and, 193
468 { Index

metamorphoses, 186 hypocrisy and, 313–14, 316, 318–19

metazoans, cellular competition in, 43–44 ideal in, 322, 329–32
microevolution, 96, 105 indirect reciprocity and, 9, 199–206,
migration, 292, 393, 430 209, 215–30, 313, 326–27, 331, 382,
Miller, Geoffrey, 431 434–35
mind. See also intelligence, evolution of indiscriminate beneficence and, 224–30,
of collective, 409–10 227f
mysteries of, 394–99 justice and, 307
play in, 9–10, 236, 271, 274–75 learning, 202
theory of, 237 motivation and, 213t, 318–20
mind’s eye, 430, 434 origin of, 308
Ming Dynasty, 367 paradoxes of, 325–33
miscalculation, of organisms, 276–77 philosophy and, 216–21, 308–16, 329,
mitosis, 48–49 332
modularity, domain-specific, 99–100 primary question of, 315–16
monarchy, 366–68 religion and, 384, 408–11
monogamy, 36–37, 190 salamanders and, 317–18
cooperation and, 43, 49–51 self-deception and, 314–19
in insects, 49 selfish behavior and, 216, 312, 319
pairs in, 49–50, 327 sex and, 311–12
rape and, 164 stages of, 223–24, 325, 327
reproductive opportunity leveling and, utilitarianism and, 326, 329
50–51 violence and, 311–12
socially imposed, 50–51, 164 warfare and, 311–12
in termites, 81 moralizing
morality corruption of, 317
Alexander and, 9–11, 199–206, 209, effectiveness of, 228, 330
215–30, 305, 307–22, 325–33 hypocrisy in, 313–14, 316
arts and, 434–35 moral systems. See also The Biology of
assessment of, 202–3 Moral Systems
biology and, 309–11, 314, 325–33 as indirect reciprocity systems, 221–22,
capacity for, 409–11, 419–20 228
competition and, 312–13 natural history of, 326–27
concealed ovulation and, 307 philosophy and religion as, 325, 331–32
conflicts of interest and, 216–21, 325, reproductive opportunity leveling and,
327–29 48
convolution of, 409 mothers
cooperation and, 318 in father-mother competition, 85–86
defined, 274 parental care from, 319–20
degrees of, 330 motivation
direct reciprocity and, 327, 434–35 in arts, 432
fish and, 317–18 consciousness and, 432
genes and, 312–13 hidden, 432–33
God and, 408–11 morality and, 213t, 318–20
harsh analysis of, surviving, 317–21 natural selection and, 288, 408–9
human evolution and, 9–11, 305, 307– Moulin, Sylvie, 139
22, 325–33 movies, 402
 Index } 469

multi-male primate bands, 160–62, 239, motivation and, 288, 408–9

263, 293 rules for applying, 250–51
multiple-queen colonies, 79, 84 scope of, 104–11
multi-regional hypothesis, 292 singular causes and, 250–51
murders, 400–404 slowness of, 415
Murdock, George Peter, 96, 96t, 113 tautological, 106–7
music, 340–41 traits and, 109–11
mutation, 108, 114–16, 250 neolocal couples, 49–50
mutualism neoteny
defined, 394 altriciality and, 176–77, 192
theories of, 40–41 childhood and, 176–78
mysteries nepotism, 74, 173, 332
causes of, 399 beneficence in, 224
of mind, 394–99 differential, 441–42
science revealing, 397–98 direct, 210t, 212, 214, 216
myths discriminative, 328–29
in arts, 414 indirect, 210t, 214, 216
self-deception and, 283 kin recognition and, 228, 331
shared, 238 risk of, 441–42
truth of, 283, 413–14, 441 nest
as resource, 81–82
naked mole-rat safe, 57, 63–67
Alexander on, 5, 12, 53, 55–59, 63–68 net-cost altruism, 393
in The Biology of the Naked Mole-Rat, 5, network and exchange theory, 325
56 neuter bees, 365–66
eusociality in, 5, 12, 53, 55–59, 63–68, New Guinea, movement to, 292
366, 375 niches, safe, 57, 63–67
fortress defense by, 57, 63–66 nonhuman animals. See also specific
hairlessness of, 191–93 animals
Nash, Ogden, 341 altriciality of, 182–88, 191–94
nations, in global harmony, 414 arts and, 429
naturalistic fallacy, 311 human evolution and, 4
natural selection indirect reciprocity among, 202,
aggression and, 125–26, 131–33 214–15
arts and, 437 primates, 147–48, 153, 157, 159–63
consciousness muted by, 394–99 tools of, 429
culture and, 98, 104–17, 120 nonostracizing humor, 355–57
Darwin and, 104–5, 259, 365, 386, 429 novelty, culture and, 97, 99–100
defined, 104
divinity and, 104–5 observation
eusociality and, 55 consciousness and, 272
genetic variation and, 107–11 learning by, 268
as guiding force of evolution, 108, 249 Observer Tit for Tat, 201
human evolution and, 105–11, 254 offspring. See also children; parent-
intelligence and, 245–97 offspring conflict and manipulation
learning and, 109–11 joint production of, 443–44
at lower levels, 250–53 selfish, 72, 85
470 { Index

On Aggression (Lorenz) parent-offspring conflict and manipulation

attention paid to, 120 Alexander on, 70–75, 77–87
review of, 2, 7, 125–28, 130–37 ecological benefits and, 74
On the Origin of Species by Means of eusociality and, 73, 77–87
Natural Selection (Darwin), 365, 386 evolution of, 70–75, 77–87
open mouth display, 338, 352 father-mother competition and, 85–86
orangutans, 147–48, 157, 159–60, 239–40, in Hymenoptera, 73, 78, 80–81, 83–85
293 in insects, 72–73, 78, 80–85
organizations, social control via, 393 kin selection and, 73–74, 77–80, 83–85
orgasm, 164–65 long-lived trees and, 82–83
ostracism role-reversal argument of, 72–73
conflicts of interest and, 346 sex ratios in, 74, 84–85
defined, 345 sterility and, 12, 77–80, 83–84, 86–87
humor and, 337–39, 341–42, 345–61 in termites, 80–82, 85
indirect reciprocity and, 345–61 parents. See also fathers; mothers
significance of, 345–46 doctors and, 218–19
status and, 346 effort of, 210t
otherness, 321, 409 elderly, 217–18
Otto the Great, 368–69 resources dispensed by, 72
outgroup. See ingroup/outgroup hypothesis parrot, 341
outlaw gene, 307 partial-cost play, 281
ovulation. See also concealed ovulation passerine bird, 35
cues, 141–44 paternal care
menstruation and, 142 altriciality and, 176, 184
in nonhuman primates, 157, 159–63 concealed ovulation and, 140–41, 145,
152, 156–58, 160–61, 164
pain, 347–48 hairlessness and, 165
pairs in nonhuman primates, 160–61
bonding of, 140–41 patriotism, 283, 289
monogamous, 49–50, 327 pattern changes, in evolution, 106–7
paper wasp, 82, 86–87, 139 Paul of Tarsus, 368
paradoxes, moral, 325–33 peace, 332, 361, 408, 412
parasites, 190 peanut rollers, 437, 448
parental care. See also alloparenting; peer-punishment, 204
paternal care “People! People!” (Alexander), 364
aggression and altruism in, 135 personality, 244
Alexander on, 138–48, 152–67 personal life, meaning of, 406–7
altriciality and, 176, 184, 189–90 pesticide treadmill, 128
concealed ovulation and, 7–8, 140–41, “Phantasm” (Alexander), 21
145–46, 152–67 philosophy
conflicting interests in, 71–72 defined, 309
kinship and, 138–48, 152–67 evolution and, 308–16
from mother, 319–20 as idealized moral system, 325, 331–32
prominence of, 152, 155, 162 indirect reciprocity and, 216–21
reciprocity and, 210t, 215 morality and, 216–21, 308–16, 329, 332
upright locomotion and, 165–66 phylogenetic patterns, 106–7
 Index } 471

physical helplessness. See altriciality primates, nonhuman, 147–48, 153, 157,

physical precociality, 174–76, 178 159–63. See also specific primates
physicians, conflicts of interest with, Prisoner’s Dilemma, 199–201
218–19 problem-solving
Pinker, Steven, 432 in arts, 432
planning, 273 intelligence and, 246–47, 273–74
plasticity, 36, 100 pseudo-estrus, 157
play. See also social/intellectual play pseudoreciprocity, 215
affiliative humor in, 355 psyche. See also intelligence, evolution of
full-cost, 281 consciousness and, 244, 267
intelligence and, 9–10, 236, 267–71, 274, discrepancies in understanding of,
281 275–76
learning and, 267–70 functions of, 267–76
in mind, 9–10, 236, 271, 274–75 in human evolution, 9–10, 267–90
partial-cost, 281 nature of, 267–90
as practice, 268–69, 281, 403 preoccupations of, 281–82
scenario-building and, 249 psychology, 297
status and, 222 punch line, 338
team competitions as, 403 punishment
pleasure, 347, 351, 431–32 indirect reciprocity and, 221, 331
pleiotropy, 174–78 peer, 204
polistine wasp, 66–67 rules spread by, 212t
political groups, 258, 291 puns, 357
polyandry, 36–37 pupil size, changes in, 144
polygyny, 36–37, 152 purpose, 273, 406–7
population density, 239, 292, 297
Porteus, Beilby, 401 Qin Shihuangdi, 367
positive sociality, 393–94 queen, 56, 66, 73–74, 78
postcopulatory sexual selection, 147 changeover, 49
Pound, Roscoe, 220 honeybee, 81, 86
power, balance of. See balance of power in multiple-queen colonies, 79, 84
power races, 247–48, 258–62, 294, 361, 404 paper wasp, 86–87
practice red fire ant, 307
humor as, 271 sting of, 86
play as, 268–69, 281, 403
precociality Raleigh, Walter, 371
children and, 174–76, 182–88 rape
concealed ovulation and, 188 concealed ovulation and, 163–64
defined, 174 monogamy and, 164
juveniles and, 189 in nonhuman primates, 159–60
mental, 8–9, 174, 179, 272 rapid evolution, 245
physical, 174–76, 178 Rawls, John, 5, 42–43, 217, 220
predation, group living and, 255–56, 264, “Reality and the Human Enterprise”
288 (Alexander), 232–33
predictability, 33–34 reciprocity. See also direct reciprocity;
prehistoric art, 430 indirect reciprocity
472 { Index

reciprocity. (Cont.) as idealized moral system, 325, 331–32

altruism and, 200–202, 205, 211t, 212, inclusive fitness theory and, 381, 397
214–16, 220, 223–24, 226, 346 leaders in, 386, 399
Axelrod and, 199–200 on meaning of life, 387, 406–8
Darwin and, 200, 205 morality and, 384, 408–11
discriminative, 328–29 murders and, 400–404
distinctive aspect of, 254 muting of consciousness and, 394–99,
economics and, 205–6 415
generalized, 346 mysteries of, 395–96
group living and, 442 nations influenced by, 414
Hamilton and, 199–200 reciprocity and, 332
importance of, 173 science and, 382, 385–89, 397–98, 404–5
language and, 202 self-deception and, 283
parental care and, 210t, 215 team sports and, 402–4
pseudoreciprocity and, 215 values of, 381–82
religion and, 332 warfare and, 385, 390–94, 400–404
retaliation in, 204 renegade cell lineages, 44
rewards in, 204–5, 211t repeatability, 29
risk of, 441–42 repeated games, folk theorem on, 206
selection, 444–46, 449 representational ability, 296
selfish behavior and, 209, 210t, 211, reproduction
214–16 via collateral relatives, 377–78
Tit for Tat and, 199–202, 206 competition and, 132, 254
ultrasociality based on, 48, 51 interests, 325
utilitarianism and, 216, 218–19 success in, 276, 311–13, 319, 326, 355,
red fire ant, 307 404, 433
Rehoboam, 366 reproductive division of labor, 59, 366
relatives reproductive effort, 36, 210t, 212, 215, 326
collateral, 377–78 reproductive opportunity leveling, 48–51,
in eusociality, 257–58 290
religion. See also God reproductive skew, 55
Alexander and, 12–13, 379–421 reputation
alternative explanations of, 387–88 arts and, 434–35
antiquity of, 386–89, 408 competition and, 447–48
competition and, 398–99, 402–4, 411 in economics, 206
consequences of, 381–82 indirect reciprocity and, 14, 202–4,
cooperation enhanced by, 13, 237–38, 434–35
382, 398, 411, 419 influence of, 14–15
Darwin and, 385–86 resentment, 223
defined, 381 resources
faith in, 404–5 localization of, 255
genocide and, 400–404 nest as, 81–82
global harmony and, 379–421 parents dispensing, 72
group living and, 382, 388–94 status and, 349
houses of worship in, 1, 398 women as, 239, 263–65
human evolution and, 12–13, 379–421 retaliation, 204
 Index } 473

return beneficence, 394, 418 of evolution, recentness of, 385–89

“Reverse Reciprocity” (Alexander), 197 mysteries revealed by, 397–98
rewards nations influenced by, 414
altruism and, 211t religion and, 382, 385–89, 397–98,
humor and, 340–41 404–5
in reciprocity, 204–5, 211t warfare and, 414
rhesus, 157 scientific method, 405
risk-taking, 284 seasonality, eusociality influenced by, 66
“The Role of Behavioral Study in Cricket secrets, 397
Classification” (Alexander), 25 selection. See also group selection; natural
role-reversal argument, 72–73 selection; sexual selection; social
Rome, 367 selection
rules concealed ovulation and, 141–42,
for applying natural selection, 250–51 157–58
evolutionarily stable decision, 59 diversity of behavior and, 29, 34–35
indirect reciprocity and, 212t, 223–24 against errors, 277
origin of, 212t, 223–24 family method of, 376
punishment spreading, 212t at individual level, 2
scenario-building and, 249 interspecies, 252
for writing about human evolution, 173 kin, 46, 59, 73–74, 77–81, 83–85, 236–
runaway intellect, 245, 293 37, 377, 420
runaway sexual selection, 261, 436, 443–44 process of, 115–16
runaway social competition, 247–48, reciprocity, 444–46, 449
258–62, 294 self-awareness
runaway social selection, 97–98, 436–37, concealed ovulation and, 166–67
442–46 as distinctive human attribute, 153
as override, 346
sacred topics, jokes on, 359 self-deception
safe niches, 57, 63–67 ability to deceive and, 166–67
Sahlins, Marshall, 441 altruism and, 314
salamanders, 317–18 arts and, 432–33
Samuel, 366–67 concealed ovulation and, 166–67,
Saul, 366–67 282–83
scenario-building humor and, 360
in arts, 433–34, 441 intelligence and, 249, 274, 281–84
humor enhancing, 340, 360 intergroup conflict and, 283–84
intelligence and, 99, 248–49, 267, morality and, 314–19
270–75 myths and, 283
language and, 290 religion and, 283
play and, 249 in risk-taking, 284
rules and, 249 scenario-building and, 249
social, 99, 248–49 sincerity and, 281
surrogate, 248–49, 271–72, 274 self-interest, 281
schemata, 267, 271, 273 selfish behavior
science evolution based on, 416
arts and, 451 intention and, 318
474 { Index

selfish behavior (Cont.) social competition, runaway, 247–48,

morality and, 216, 312, 319 258–62, 294
of offspring, 72, 85 social control, via organizations, 393
reciprocity and, 209, 210t, 211, 214–16 social Darwinism, 310
The Selfish Gene (Dawkins), 200, 235 social evolution
selfish herds, 255, 257 classical theory of, 40
selflessness, consciousness and, 418 concealed ovulation and, 152–67
self-understanding, 408, 415, 418, 420, 437, insects and, 21–37, 77–87
451 social hustling, 221–22
semen, 147–48 social/intellectual play
senescence theory, 175, 177–79 in arts, 433–34
sense of humor, 340, 352–53 intelligence and, 236, 248, 270–71, 274,
sex 281
differences in humor, 353 social investment, 393, 418–19
morality and, 311–12 sociality
ratios, 74, 84–85 atoms of, 209–16, 210t–213t
sexual competition, 158, 431 in canines, 256–57
sexual dimorphism, 431 consciousness and, 267
sexually asymmetrical traits, 140, 152–54 in felines, 256–57
sexual receptivity, continuous, 157–58, 163 group living and, 255
sexual response, during menstrual cycle, intelligence and, 237, 240–41, 244–49,
144, 148 255, 281
sexual selection, 134, 248, 317 positive, 393–94
of arts, 430–32 socially imposed monogamy, 50–51, 164
postcopulatory, 147 socially mediated nepotism. See indirect
runaway, 261, 436, 443–44 nepotism
social selection distinguished from, 435, socially mediated somatic effort. See
443–44 indirect somatic effort
shaggy dog stories, 357 social organization, of chimpanzees, 160–
Shakespeare, William, 341 61, 263, 293
sham estrus, 162–63 social prowess, 222
Shang Dynasty, 367 social scenario-building, 99, 248–49
shared myths, 238 social scrutinizing, 202
Sherman, P.W., 5, 56 social selection
Sima Qian, 371 arts and, 429–37, 442–46, 451
sincere hypocrisy, 360 culture and, 97–98, 442–46
sincerity, 281, 360 defined, 432
singing male field cricket, 23, 23f runaway, 97–98, 436–37, 442–46
single-locality hypothesis, 292 sexual selection distinguished from,
single-male primate bands, 160 435, 443–44
singular causes, 250–51 social skills, in arts, 440–41
skew theory, 74–75 social structure, aggression and, 134–35
slapstick humor, 338 social unity. See unity
smiling, 338, 351–53 sociobiology, 109, 235
Smith, John, 371 socioecology models, of great apes, 239–40
Smith, Maynard, 44, 377 Solomon, 366–67
Social Brain Hypothesis, 237, 240–41 somatic effort
 Index } 475

direct, 209, 210t, 211, 215 systematics

indirect, 210t, 211–12, 215–16 comparative animal behavior and, 26,
somatic environments, 177–78 29–37
song patterns, of birds, 35 evolution and, 24
South America, movement to, 292 predictability in, 33–34
speciation, 106–7
sperm taboos, menstrual cycle, 145–46
intra-ejaculate competition of, 44–45 tactical deception, 236–37
mating effort and, 212 tautological natural selection, 106–7
postcopulatory sexual selection and, 147 taxonomy
status comparative method and, 31
arts and, 434–35, 441–42, 446 cricket, 23–26, 23f
defined, 349 team competitions, in sports, 402–4
effects, 349–51 technology, 262, 449–50
extremes and, 446 termite colonies
humor and, 337–39, 349–60 competition suppressed in, 45
importance of, 441–42 diploid males in, 80
ostracism and, 346 monogamy in, 81
play and, 222 nest as resource for, 81–82
resources and, 349 parent-offspring conflict and manipula-
shifts, 271 tion in, 80–82, 85
tricks lowering, 350 safe niche of, 63, 65, 67
sterility The Territorial Imperative (Ardrey)
Darwin and, 77–78, 365–71, 375–77 attention paid to, 120
democracy and, 369 review of, 2, 7, 125–28, 130–37
ecological constraints and, 365–71 testosterone, 143
evolution of, 12, 77–80, 83–84, 86–87 theater
humans and, 366–71 arts as, 440–41
inclusive fitness theory and, 376–77 interest in, 347
in insects, 12, 77–80, 83–84, 86–87 theocracy, 368–69
monarchy and, 366–68 theory of interest, 325–27
of neuter bees, 365–66 theory of mind, 237
in parent-offspring conflict and manip- threats, in aggression, 132
ulation, 12, 77–80, 83–84, 86–87 three-point hitch, 449–50
theocracy and, 368–69 tickling, 351–52, 354–55
storytellers, 440 Tinkle, Donald, 2, 7, 30, 36, 125–28,
strong inference, 141 130–37
subconscious, deception and, 282–83 Tit for Tat, 199–202, 206
success “To a Life Mate” (Alexander), 138
relative nature of, 328, 355, 434 tools
reproductive, 276, 311–13, 319, 326, development and use of, 153, 240, 247
355, 404, 433 of nonhuman animals, 429
supernaturalism, 413 visualization of, 430
superoptimal stimulus effect, 446 weapons, 294–95
surrogate scenario-building, 248–49, traits
271–72, 274 genetic variation and, 109–11
symbolism, 117–18 hidden, 399
476 { Index

traits (Cont.) group selection and, 205

natural selection and, 109–11 human evolution influenced by, 291,
sexually asymmetrical, 140, 152–54 294–96
trees, long-lived, 82–83 intelligence and, 239, 246, 265
trickle-down effect, 118 morality and, 311–12
tricks, 338, 350, 358 prevalence of, 417
trigger strategies, 206 religion and, 385, 390–94, 400–404
Trivers, Robert, 2, 200 science and, 414
tropical paper wasp, 82 tickling and, 354–55
truth, 249, 283, 413–14, 441 wasps, 66–67, 73, 82, 86–87, 139
weapons
ultrasociality, 48, 51 expansion of, 402, 414, 420
unity tools as, 294–95
continuity of, 332 western films, 402
God as metaphor for, 381–83, 410, 418 Western Pleasure horse competitions,
universality, of God, 408–11, 419 448
University of Cape Town, 55 “What Do Children Owe Elderly Parents?”
University of Michigan, 2, 56, 145, 220, 395 (Callahan), 217–18
upright locomotion, 165–66 What Is Justice? (Kelsen), 220
utilitarianism Wheeler, William Morton, 29
culture and, 112 white-handed gibbons, 159
egoism and, 10–11, 326 Williams, George
genetic altruism and, 252–53 influence of, 2, 71, 125, 178, 250
indiscriminate beneficence and, 225 on intellect, 189
morality and, 326, 329 on selfishness, 416
reciprocity and, 216, 218–19 Wilson, Ed, 235
winners, 449
values, of religion, 381–82 wit, 350–51, 353
veil of ignorance, 42 within-group cooperation
vertebrate eusociality, 65–68, 365–66 Alexander and, 14–15, 123, 125–28,
violence. See also warfare 130–37
deaths from, 400–401, 404 in families, 134
genocides and murders, 400–404 intergroup competition and, 14–15, 123,
morality and, 311–12 125–28, 130–37
visualization, in arts, 430, 434 Wittgenstein, L., 309
vulnerability, 397 women
orgasm of, 164–65
warfare as resources, 239, 263–65
aggression in, 125–27, 133, 135–37, 293 sexual receptivity of, 157–58, 163
causes of, 401 worker ants, 55
competition and, 239 worship, houses of, 1, 398
deaths from, 400 written records, 295
development of, 296
emotions in, 289 Yanomamo, 147
global harmony and, 385, 390–94,
414–19 zoologists, 32