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BIOLOGICAL SYSTEMATICS

Principles and Applications

Third Edition

Andrew V. Z. Brower
National Identification Services, Plant Protection and Quarantine,

Animal and Plant Health Inspection Service, United States

Department of Agriculture, Riverdale, Maryland; Research

Associate, Division of Invertebrate Zoology, American Museum

of Natural History, New York, New York; and Department of

Entomology, National Museum of Natural History, Washington,

District of Columbia

Randall T. Schuh
George Willett Curator of Entomology Emeritus, Division of

Invertebrate Zoology, and Professor Emeritus, Richard Gilder

Graduate School, American Museum of Natural History, New

York, New York; Adjunct Professor Emeritus, Department of

Entomology, Cornell University, Ithaca, New York; and

Department of Biology, City College, City University of New

York, New York

COMSTOCK PUBLISHING ASSOCIATES

AN IMPRINT OF CORNELL UNIVERSITY PRESS ITHACA AND

LONDON
Contents

Preface to the First Edition

Preface to the Second Edition

Preface to the Third Edition

Acknowledgments to the First Edition

Acknowledgments to the Second Edition

Dedication and Acknowledgments to the Third Edition

Section I HISTORICAL AND PHILOSOPHICAL BACKGROUND FOR

SYSTEMATICS

1. Introduction to Systematics: First Principles and Practical

Tools

2. Systematics and the Philosophy of Science

Section II CLADISTIC METHODS

3. Characters and Character States

4. Character Polarity and Inferring Homology

5. Tree-Building Algorithms and Philosophies

6. Evaluating Results

Section III APPLICATION OF CLADISTIC RESULTS

7. Species: Concepts, Recognition, and Analytical Problems

8. Nomenclature, Classifications, and Systematic Databases

9. The Integration of Phylogenetics, Historical Biogeography,

and Host-Parasite Coevolution

10. Evaluating Hypothetical Scenarios of Evolution, Ecology

and Adaptation

11. Understanding Molecular Clocks and Time Trees

12. Biodiversity and Conservation

Postscript: Parsimony and the Future of Systematics

Appendix

Glossary

Literature Cited

Author Index

Subject Index
Preface to the First Edition

All fields of science have undergone revolutions, and systematics is no

exception. For example, the discovery of DNA structure fundamentally

altered our conception of the mechanisms of inheritance. One might

assume that the most recent revolution in systematic biology would have

come about through the proposal of a coherent theory of organic evolution

as the basis for recovering information on the hierarchic relationships

observed among organisms. Such was not the case, however, no matter the

frequency of such claims. Rather, it was the realization by Willi Hennig—

and others—nearly one hundred years after the publication of the Origin of

Species by Charles Darwin, that homologies are transformed and nested, and

that phylogenetic relationships can best be discovered through the

application of what have subsequently come to be called cladistic methods.

The fact that the theory of evolution allowed for the explanation of a

hierarchy of descent was seemingly not sufficient to arrive at a method for

consistent recovery of genealogical relationships. It can further be argued

that neither was it necessary.

The revolutionary changes did not stop there, however. At the same time

that the methods of cladistics were changing taxonomic practice on how to

recognize natural groupings, the issue of quantification was being discussed

with equal fervor. Whereas systematics was long a discipline marked by its

strong qualitative aspect, the analysis of phylogenetic relationships is now

largely quantitative.

The introduction of quantitative methods to systematics began with the

“numerical taxonomists.” Their approach to grouping was based on overall

similarity concepts, and the attendant assumption of equal rates of

evolutionary change across phyletic lines. Establishment of systematic

relationships is now dominated by cladistic methods, which form groups on

the basis of special similarity and allow for unequal rates of evolutionary

change. The logic and application of quantitative cladistics were in large

part developed by James S. Farris.

The overall approach of this book is to present a coherent and logically

consistent view of systematic theory founded on cladistic methodology and

the principle of parsimony. Some of its subject matter is in a style that

would commonly be found in research papers, that is, argument and

critique. This approach allows material to be presented in its unadulterated

form rather than in the abstract, such that sources of ideas at which

criticism is being directed are not obscured and can be found readily in the

primary literature. The tradition of critical texts in biological systematics

was established by Blackwelder, Crowson, Hennig, Sokal and Sneath, and

others. I hope that the style of this book will help students see

argumentation in science for what it is, a way of developing knowledge and

understanding ideas. The alternative would be to obscure historical fact by

pretending that the formulation of a body of critical thought has proceeded

in a linear fashion, without sometimes acrimonious debate.

Organization of the Text. This work is divided into three sections,

representing more or less logical divisions of the subject matter. Section 1,

Background for the Study of Systematics, comprises three chapters, which

offer, respectively, an introduction to biological systematics, binominal

nomenclature, and the philosophy of science as applied to systematics.

Section 2, Cladistic Methods, outlines the methods of phylogenetic analysis,

with chapters on homology and outgroup comparison, character analysis,

computer-implemented phylogenetic analysis, and evaluation of

phylogenetic results. Section 3, Application of Cladistic Results, comprises

chapters on the preparation of formal classifications, historical

biogeography and coevolution, testing evolutionary scenarios, and

biodiversity and conservation. A terminal glossary provides definitions for

the specialized terminology of systematics used in this book.

Each chapter ends with lists of Literature Cited and Suggested Readings.

The references cited in the text are those actually needed to validate an

argument, but do not in all cases necessarily represent the most useful
available sources. The Suggested Readings are intended to augment the

material presented in the text with more detailed knowledge to challenge the

more sophisticated and inquiring student. The readings are chosen for their

breadth and quality of coverage, with consideration also being given to their

accessibility. Most should be available in major university libraries, and thus

be readily available to most students and professors using this book.

R. T. Schuh, 2000
Preface to the Second Edition

Nearly a decade has passed since the publication of the first edition of

Biological Systematics. Computers have become faster, phylogenetic data

matrices have become larger, and presentation of phylogenetic trees has

become commonplace, even in literature outside the traditional realm of

systematics. The exponential growth of DNA sequence data production has

led to the emergence of the new disciplines of genomics and bioinformatics.

During this interval, however, the core principles of systematics—discovery

and interpretation of characters, construction of data matrices, search for

most parsimonious trees—have remained largely unaltered. Therefore, our

revision incorporates philosophical and technical advances of the past ten

years, but also elaborates and enhances with additional examples the ideas

that have formed the basis of modern systematics since its origins nearly

fifty years ago.

Although likelihood-based methods of phylogenetic inference have

increased in popularity, perhaps due to their implementation in easy-to-use

software packages, our book retains its cladistic emphasis. As we have each

found in our respective empirical research on Hemiptera and Lepidoptera,

the cladistic approach is the most transparent, flexible, and direct means to

interpret patterns of character-state transformation as evidence of

hierarchical relationships among taxa. The most vociferous advocates of

alternative methods are not biologists, but statisticians and computer

programmers. We have been accused of “bias” in our preference for

cladistic methods over alternatives, but we think—and endeavor to explain

in the book—that our methodological choices are based on a clear and

objective understanding of the problem being addressed. Systematics is not

just about tree-building algorithms; our book devotes just one of its ten

chapters to that aspect of the discipline. It is, rather a world view, nothing
less than a coherent approach for organizing and understanding

information about the natural world. It is with that idea in mind that we

have chosen our subject matter and organized our overall presentation.

Reorganization of the Text. We have revised and expanded the entire book,

although its overall structure remains largely the same as the first edition.

Chapter 1 reviews the history of modern systematics and philosophical

differences among various schools. Chapter 2 addresses philosophical

underpinnings. An extensively reorganized discussion of character coding

and homology is addressed in Chapters 3 and 4. Chapter 5 covers tree-

building methods and offers an expanded discussion and critique of the

rationale and methods of maximum likelihood, and Chapter 6 describes

methods for assessing support for resultant topologies. The discussion of

biological nomenclature has been moved to Chapter 7, and merged with an

expanded critique of “phylogenetic nomenclature” and the Phylocode.

Chapters 8, 9, and 10 examine applications of cladistic results to

biogeography, ecology, and biodiversity, respectively. All of the works cited

are listed at the end of the book in a comprehensive Literature Cited section,

rather than at the end of individual chapters, as in the first edition. Each

chapter is accompanied by a supplementary list of Suggested Readings,

which represents a cross-section of classic and recent articles and books

intended to provide background and deeper understanding of relevant

issues. The glossary of terms at the back of the book has been expanded and

revised.

R. T. Schuh and A. V. Z. Brower

Preface to the Third Edition

Another decade has passed since the second edition of Biological Systematics

appeared, and the changes to systematic biology we described in our 2009

preface continue to unfold. Our discipline has proceeded into an era of

incomprehensibly large molecular data sets, with automated pipelines to

assemble matrices for comparative genomics, and a growing skepticism in

some quarters that relationships among the diversity of living things are

straightforwardly represented by “a tree.” Although it is hard to object to

larger data sets as more comprehensive evidentiary bases for phylogenetic

inference, and although we appreciate that the scope of “big data” means

that some automation is inevitable and perhaps benign (just as tree-

searching has been facilitated by computers), we find that data enormity

comes at a price: we are alarmed by the degree to which defective systematic

methods, discarded long ago, have been resurrected in the workflows of

contemporary phylogenomics. It is clear from the literature that many

contemporary workers embrace a bioinformatic operationalism that no

longer concerns itself with the fundamental principles that have underlain

systematics during preceding centuries, and particularly since the Hennigian

revolution of the 1970s. Researchers may be adept at pushing buttons, but

we think they ought also to understand why they push the ones they do and

what assumptions underlie those choices.

The aim of this book, as it has been through the previous editions, is to

offer a theoretically coherent roadmap to aid navigation of this vast data

landscape—one that not only advises the reader which turns to take but also

explains why some routes are better than others. Our goal remains to

explicate the theoretical grounds for interpreting the form and meaning of

biosystematic evidence, for understanding how that evidence is used to infer

patterns of relationship among taxa, and for applying those patterns to

inform other aspects of comparative biology. To this end, now more than

ever, we maintain and continue to advocate the cladistic approach.

We are cladists, and we do not refrain from advocating our

methodological preferences and noting contrasts with alternative

viewpoints. A number of the methods described in the book have been in

use for several decades, but venerability is not per se a legitimate criticism of

a methodology’s philosophical soundness and ongoing utility. Fundamental

concepts such as homology, the irregularly bifurcating hierarchy, and the

principle of parsimony have been with us for centuries or millennia, yet

remain critical elements of the conceptual framework of biological

systematics. For that matter, we might observe that popular alternative

frameworks are hardly recent innovations: maximum likelihood was

conceived by Ronald Fisher nearly 100 years ago and was applied to

phylogenetic questions in the early 1960s. Bayes’ Theorem was published in

1763.

You may have read—perhaps on a social media site—that cladistics is

old-fashioned, Luddite, or even utterly irrelevant to modern phylogenetic

studies, and that the people who still employ its methods are irrational

zealots, like acolytes of a religious cult. We are prepared—indeed,

enthusiastic—to defend cladistics against sober and legitimate criticisms,

but naturally, we find such ad hominem stuff to be puerile and without

substance. A religion is a system of metaphysical beliefs without a firm

empirical foundation. This book is all about the empirical foundations of

systematics and about questioning metaphysical suppositions. One of its

take-home messages is that quantitative complexity does not equate to

explanatory robustness. In fact, as any statistician can tell you, just the

opposite is true. The approach we endorse values empirical clarity and

methodological transparency between evidence and inference—in short,

parsimony.

What’s new in the third edition? We have updated the entire book, with

major revision to Chapters 1 and 2. We have added two new chapters, one

addressing species concepts and issues related to phylogenetic inference at

its lower bound, and another on understanding molecular clocks. We have

significantly expanded the glossary, as well. (Note that, as has been the case

through all editions of the book, terms italicized in the text are defined in

the glossary). The numerous systematics resources available on the web that

we cite in the text are listed in the reference section with current URLs.

These are indicated to be web resources in the text with the parenthetical

statement “(online).”

Since the publication of the previous edition of Biological Systematics,

new or revised editions of several other systematics-related texts have

appeared. Because this book will not be to everyone’s taste, and because a

circumspect systematist should always strive for a clear understanding of the

breadth of opinions in the field, we offer the following list of books for the

reader’s awareness, edification, and/or amusement:

Baum, D.A., and S.D. Smith. 2013. Tree Thinking: An Introduction to Phylogenetic

Biology. Greenwood Village, CO: Roberts.

Bromham, L. 2016. An Introduction to Molecular Evolution and Phylogenetics, 2nd ed.

Oxford: Oxford University Press.

Chen, M.H., L. Kuo, and P. Lewis, eds. 2014. Bayesian Phylogenetics: Methods, Algorithms,

and Applications. Boca Raton, FL: Chapman and Hall/CRC Press.

Warnow, T. 2018. Computational Phylogenetics: An Introduction to Designing Methods

for Phylogeny Estimation. Cambridge: Cambridge University Press.

Wheeler, W.C. 2012. Systematics: A Course of Lectures. Chichester, UK: Wiley–Blackwell.

Wiley, E.O., and B.S. Lieberman. 2011. Phylogenetics: Theory and Practice of Phylogenetic

Systematics. Hoboken, NJ: John Wiley and Sons.

Yang, Z. 2014. Molecular Evolution: A Statistical Approach. Oxford: Oxford University

Press.

Zander, R.H. 2013. A Framework for Post-Phylogenetic Systematics. St. Louis: Zetetic

Publications.

It is the responsibility of all scholars to understand the premises and

assumptions of their chosen methodologies. Even if you disagree with our

approach to systematics, we hope that this book provokes you to think

about the reasons why.

A. V. Z. Brower and R. T. Schuh

Acknowledgments to the First Edition

Several colleagues and friends provided discussion, assistance, advice,

reviews, and encouragement during the course of writing this book. For

reviews of an early version of the manuscript, or parts thereof, I thank James

Ashe, Gerasimos Cassis, David Lindberg, Steven Keffer, Norman Platnick,

James Slater, Christian Thompson, Quentin Wheeler, and Ward Wheeler.

For reviews of the complete manuscript, I offer special thanks to Andrew

Brower, James Carpenter, Eugene Gaffney, Pablo Goloboff, Dennis

Stevenson, and John Wenzel. Dennis Stevenson gave me much advice on

botanical examples and nomenclature, and offered some very timely

encouragement as this project progressed. My conception of issues of

philosophy and systematic theory, as presented in this volume, has been

influenced by discussions with Andrew Brower, James Carpenter, Eugene

Gaffney, Pablo Goloboff, and Norman Platnick. Pablo Goloboff was

immensely helpful in clarifying my presentation of the quantification of

cladistics. Gregory Edgecombe offered suggestions on relevant literature.

The students and auditors in my Spring 1998 Principles of Systematics

course at the City University of New York field-tested a version of the

manuscript. Christine Johnson read and commented on the final

manuscript and prepared the figures. Whatever the inputs from others, in

the end, I am solely responsible for the final form of all arguments presented

in the text.

The development of my views on the nature of systematics was shaped by

two people in particular, my long-time friends and colleagues James S.

Farris and Gareth Nelson. Since 1967, they, more than any other

individuals, have profoundly affected our understanding of systematic

theory. Thus, in an indirect way, they have greatly influenced the way I have

written this book.

 The encouragement of my wife, Brenda Massie, and Steven Keffer caused

me to go to work on this project. Their confidence that I could produce a

useful final product spurred me on. My young daughter, Ella, has been a

patient helper during the preparation of the manuscript. The term

‘systematics’ is now indelibly imprinted in her mind.

Randall T. Schuh

New York, October 1998

Acknowledgments to the Second Edition

This edition of Biological Systematics is co-authored by Andrew Brower, a

systematic entomologist whose research is focused on the phylogenetic

relationships of nymphalid butterflies. Andy’s training as a systematist

began at Cornell University and continued at the American Museum of

Natural History and the Smithsonian Institution. He is extremely grateful to

his colleagues and mentors at these institutions for providing a collegial and

scholarly environment that gave him the opportunity to develop his

perspectives on the discipline. Access to a free copier in a great library is a

wonderful thing. As the Rice Professor of Systematic Entomology, Andy

taught a graduate course in Principles of Systematics at Oregon State

University between 1998 and 2005, an experience that helped him develop

an organized framework for training systematics students. He thanks

Harold and Leona Rice for their generous support of his systematics

research and training program. He would like to acknowledge Darlene Judd

for her systematic insight and moral support. He would also like to thank

Randall “Toby” Schuh for the opportunity to contribute to this revision of

the first edition. Both authors are grateful to Marc Allard and two

anonymous reviewers of the revised manuscript for their thoughtful

comments. We thank also Gerasimos Cassis, Dimitri Forero, James S.

Miller, Mark E. Siddall, F. Christian Thompson, Ward C. Wheeler, and

David M. Williams for discussion of our approach, comments on portions

of the manuscript, or for other assistance. Once again we acknowledge

Pablo Goloboff for his contributions to issues relating to the quantification

of cladistics in the first edition, because we continue to use much of that

material in the revised version.

Randall Schuh, New York

Andrew Brower, Murfreesboro, Tennessee

December 2008
Dedication and Acknowledgments to the Third Edition

As we were checking the copyedited version of the manuscript for the third

edition, we learned that our longtime colleague and friend, Norman I.

Platnick, had suffered a mortal injury that eventually ended his remarkable

life at the age of sixty-eight. Norman was a person of prodigious intellect

who joined the curatorial staff of the American Museum of Natural History

in New York City, Harvard Ph.D. in hand, at the age of twenty-one. Over

the course of the next 40 years he became one of the most influential spider

specialists of all time. As readers of this work will find, he also had a

profound impact on the relationship of the philosophy of science to

systematics, the theory and practice of phylogenetic systematics, and

historical biogeography. It is in recognition of his seminal contributions to

the field that we dedicate this third edition of Biological Systematics to his

memory.

We thank Kitty Liu and the staff of Cornell University Press for their

willingness to publish a third edition of our book and two anonymous

reviewers who provided frank opinions and valuable suggestions on the

manuscript, many of which we have incorporated into the revision. We

thank Jennifer Savran Kelly and Eva Silverfine for meticulous copyediting,

reference checking, and thoughtful suggestions to improve the flow of the

text.

Andy is grateful to former colleagues at Middle Tennessee State

University and new colleagues at the United States Department of

Agriculture, Animal and Plant Health Inspection Service, Plant Health

Programs for their friendship and support, and in particular to the National

Identification Service for bringing him aboard as a supervisor of the

National Taxonomists (the specialists responsible for final authoritative

identification of potential pests and pathogens intercepted at US ports of

entry by US Customs and Border Protection inspectors). Precise, accurate,

and timely identification of potential quarantine pests is where the

systematic rubber hits the road, and after an academic career in pursuit of

butterfly phylogeny, Andy is excited to be a part of this practical endeavor to

protect global agriculture via applied regulatory biogeography. Many of the

changes to the new edition of the book were composed on the Brunswick

Line of the MARC train (not on “government time”). Nevertheless, it is

prudent to assert, “The opinions expressed in this book do not necessarily

represent the policies or views of the US Department of Agriculture or the

United States Government.

Randall Schuh, New York, and Andrew Brower, West Virginia

Section I
HISTORICAL AND

PHILOSOPHICAL BACKGROUND

FOR SYSTEMATICS
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