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 ENCYCLOPEDIA OF
EVOLUTIONARY BIOLOGY
 ENCYCLOPEDIA OF
EVOLUTIONARY BIOLOGY

EDITOR IN CHIEF

RICHARD M. KLIMAN
Cedar Crest College, Allentown, PA, USA

VOLUME 1
Academic Press is an imprint of Elsevier
The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB
225 Wyman Street, Waltham MA, 02451

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Printed and bound in the United States of America

16 17 18 19 20 10 9 8 7 6 5 4 3 2 1
EDITOR IN CHIEF

Richard M. Kliman, PhD, is Professor of Biological Sciences at Cedar Crest College in

Allentown, Pennsylvania. He received his BA from Colby College in biology and music. His
graduate work at Wesleyan University focused on quantitative genetics of circadian rhythms
and photoperiodism in the Djungarian hamster, Phodopus sungorus. As a postdoctoral fellow
at Rutgers University and Harvard University, he studied molecular evolution and popu-
lation genetics. Prior to Cedar Crest College, he taught at Radford University in Virginia and
Kean University in New Jersey. He has also served as a program director in the Division of
Environmental Biology at the US National Science Foundation (NSF).
Kliman’s research interests center on questions in molecular evolution, including the
evolution of codon usage bias in a variety of organisms; speciation and natural history; and
ecology and conservation. Much of this work has relied on population genetics/genomics
and bioinformatics approaches. He has also collaborated with Cedar Crest colleague John
Cigliano on an Earthwatch-supported “before-after-control-impact” study on the effects of a
new marine reserve in Belize on queen conch populations. His research in evolutionary and
ecological genetics has been supported by the US National Institutes of Health and by
Conservation International.
Kliman has served on the editorial boards of Genetica and The Journal of Molecular Evolution. He has been deeply involved in
evolution education, helping to coordinate “Undergraduate Diversity at SSE/SSB,” an NSF-supported program to bring a diverse
group of undergraduates to the annual Evolution research conference. He was a lead editor of population/quantitative genetics
and evolutionary genetics for Nature Education/Scitable at its inception. He is a member of the Education and Outreach Committee
of the Society for the Study of Evolution, and editor of the society’s peer-reviewed educational resource, the EvoEd Digital Library.

v
SECTION EDITORS

Hiroshi Akashi is a Professor of Evolutionary Genetics at the National Institute of Genetics,

Japan. He worked with Marty Kreitman for his PhD in Ecology & Evolutionary Biology from
the University of Chicago (1996) and with John Gillespie as a postdoctoral fellow at UC
Davis. He has been a faculty member at the University of Kansas (1998–2000), Penn State
University (2000–2008), and NIG (2009–present). Akashi’s research focuses on inferring
causes of genome evolution, especially weak selection, from within and between species
sequence variation. His studies of codon usage employed population genetic methods to
detect natural selection acting at its limit of efficacy and identified a phenotypic basis of
natural selection (translational accuracy) from sequence comparisons in Drosophila. Exten-
sions of this work revealed constraints related to biosynthesis that act globally on com-
positional properties of microbial proteins. The interplay of weak evolutionary forces
appears to shift frequently among closely-related species and current interests include tests
of adaptive changes in protein/DNA composition.

Tim Coulson’s primary interest is in creating better links between the fields of ecology and
evolution. He does this by developing theory, parameterising models for field and laboratory
systems, making predictions from these models, and, where possible, testing these predic-
tions with experiments. He works on a range of systems, from bulb mites within the la-
boratory, to guppies living in streams in Trinidad, to wolves in Yellowstone. His motivation
to do this comes from observations that ecological and evolutionary change can be observed
occurring on similar time scales, yet ecological theory typically ignores evolutionary pro-
cesses and vice versa.
Tim was awarded his PhD in plant ecology from Imperial College, London, in 1994. He
moved on to research genotype-by-environment interactions as Natural Environment Re-
search Council (NERC)-funded post-doc at the Institute of Zoology in London. He remained
at the Institute on a fellowship where he developed models to investigate the economic and
life history consequences of a range of population management strategies. In 2000 he moved
to the University of Cambridge, where he briefly lecturered in the Zoology department. In
2004 he moved back to Imperial College London as a senior lecturer where he started
developing models that allow the simultaneous investigation of the dynamics of life history, populations, and quantitative
characters. In 2007 he became Professor of Population Biology at Imperial College London. He left Imperial in 2013 to take up his
current position as Professor of Zoology at the University of Oxford. He is also a Professorial fellow of Jesus College, Oxford.

Andrew Forbes

vii
viii Section Editors

Rosemary Gillespie is a Professor at the University of California, Berkeley, where she also
holds the Schlinger Chair in Systematics. She is Past President of the International Bio-
geography Society and Trustee and Fellow of the California Academy of Sciences, and serves as
Associate Editor for Molecular Ecology. Gillespie was born and educated in Scotland, receiving
her BSc in Zoology from Edinburgh University in 1980. She came to the US to conduct
graduate work on the behavioral ecology of spiders at the University of Tennessee. After her
PhD she spent several months at the University of South in Tennessee, and then started work
at the University of Hawaii in 1987, initially as a postdoc, and then in 1992 as Assistant
Professor in Zoology and Researcher in the Hawaiian Evolutionary Biology Program. It was
during her first year in Hawaii that she discovered an adaptive radiation of Tetragnatha
spiders. She left Hawaii in 1999 to join the faculty at the University of California in Berkeley,
where she continues her research focus on the islands of the Pacific, Hawaii in particular,
using islands of known age and isolation to assess the combined temporal and spatial
dimension of biogeography and determine patterns of diversification, adaptive radiation,
and associated community assembly.

David Guttman received his PhD from Stony Brook University in 1994 working with Daniel
Dykhuizen on questions related to the role and importance of recombination in structuring
genetic diversity in bacterial populations. He followed this with a postdoc in molecular
evolution with Brian and Deborah Charlesworth at the University of Chicago, and a second
postdoc at the University of Chicago with Jean Greenberg to gain experience in the fields of
molecular plant pathology and plant-microbe interactions. He started his faculty position at
the University of Toronto in 2000, and is currently a Professor in the Department of Cell &
Systems Biology (CSB). He is also the Associate Chair for Research in CSB, founder and
Director of the University of Toronto Centre for the Analysis of Genome Evolution &
Function, and Canada Research Chair in Comparative Genomics. He has served as the Chair
of the American Society for Microbiology, Division R (Evolutionary and Genomic Micro-
biology), and was the PLoS Pathogens Section Editor for Bacterial Evolution & Genomics.
Dr. Guttman runs a highly diverse research program generally focused on bacterial
evolutionary genomics, with three major foci: (1) the evolution of host specificity and
virulence in plant pathogenic bacteria; (2) microbial comparative genomics; and (3) studies
of the human and plant-associated microbiome. He is best known for elucidating and
linking evolutionary and mechanistic processes that determine the course and fate of bac-
terial infections, and characterizing the impact of genetic variation on the balance between
disease and immunity.

Norman A. Johnson, the section editor for Applied Evolution, is an evolutionary geneticist
and author. He received his PhD from the University of Rochester in 1992 and did post-
doctoral research at the University of Chicago. His research interests have generally focused
on aspects of speciation, specifically those related to the genetics and evolution of hybrid
incompatibility: sterility, inviability, or other reduction of fitness in hybrids between species.
Dr. Johnson, an adjunct professor in the Biology Department at the University of Massa-
chusetts at Amherst, has taught classes there, as well as at Hampshire College, the University
of Texas at Arlington, and the University of Chicago.
Dr. Johnson also has a long-standing commitment toward improving the communi-
cation of science in general and evolutionary biology in particular to other scientists, edu-
cators, and the public at large. He is the author of Darwinian Detectives: Revealing the Natural
History of Genes and Genomes (Oxford University Press: 2007), a book geared to general
audiences that shows how biologists use DNA sequence data to make inferences about
evolutionary processes. He also was the lead organizer for a working group on communi-
cating human evolution at the National Evolutionary Synthesis Center (NESCent).
 Section Editors ix

Laura Kubatko received a PhD in Biostatistics from The Ohio State University (OSU) in
1999. After seven years on the faculty at the University of New Mexico, she returned to OSU
in the Fall of 2006, and is now Professor of Statistics and of Evolution, Ecology, and
Organismal Biology at OSU. Laura served as an Associate Director of the Mathematical
Biosciences Institute at OSU from 2013–2015. At OSU, she is a Faculty Affiliate of the
Initiative in Population Research, and a Faculty Affiliate in Translational Data Analytics
(TDA@OSU). She holds appointments as an Affiliate Faculty Member at the Battelle Center
for Mathematical Medicine at Nationwide Children’s Hospital in Columbus and as an Ad-
junct Research Scientist at Lovelace Respiratory Research Institute in Albuquerque, NM.
Laura’s research interests are in statistical genetics, with a focus on the development of
statistical methods for inferring phylogenies from molecular data. Her recent work in this
area concentrates on bridging the gap between traditional phylogenetic techniques and
methodology used in population genetics analyses, primarily through the application of coalescent theory to species-level
phylogenetic inference. She develops and distributes several software packages for phylogenetic inference, and has been an active
member of the Society of Systematic Biologists. She has served as an Associate Editor for the journal Systematic Biology since 2007.

Amy Litt has been studying plant evolution and diversity since her PhD on floral structure
and evolution in the neotropical plant family Vochysiaceae, known for its beautiful but
unusual flowers many of which have only one petal and one stamen. While completing her
PhD in plant systematics and morphology in the joint City University of New York/New
York Botanical Garden Plant Sciences program under Scott Mori and Dennis Stevenson, she
became interested in the molecular basis of plant diversity. She did her post-doc in the
developmental genetics lab of Vivian Irish at Yale University on the evolution of a family of
transcription factors involved in flower development, and she continues to study the func-
tional evolution of this gene family currently. After one year on the faculty of University of
Alabama, she moved back to The New York Botanical Garden as Director of Plant Genomics,
where she developed her research program studying the evolution of plant form along two
paths: studying evolutionary changes in genes to see how those changes affected flower and
fruit form; and identifying the genes that underlie differences in form among closely related
species. Dr. Litt also served as a program director in Plant, Fungal, and Microbial Devel-
opment and Evolutionary Development at the National Science Foundation. She recently moved to the University of California at
Riverside, where she continues to study the genetic basis of plant diversity.

Maria E. Orive is a professor of evolutionary genetics in the Department of Ecology and

Evolutionary Biology at the University of Kansas. Her research in theoretical population
genetics aims to develop mathematical models that provide a conceptual framework for
exploring important questions in evolutionary biology and analytical tools for demographic
and genetic data. Her work has considered levels of selection and mutation in organisms that
reproduce both sexually and asexually, the relationship of population structure and life-
history attributes to gene flow and genetic diversity, and models of within- and between-host
pathogen and symbiont population dynamics. Orive received her BS from Stanford Uni-
versity and her PhD from the University of California at Berkeley. After spending two years as
a postdoctoral researcher in genetics at the University of Georgia, she was an NSF-NATO
Postdoctoral Fellow at the University of Edinburgh. Her research has been funded by
multiple grants from NSF and NIH. In 2007–2008, she was the Carl and Lily Pforzheimer
Foundation Fellow at the Radcliffe Institute for Advanced Study (Harvard University), and
has served as the University Faculty Ombudsman for the University of Kansas since 2007.
x Section Editors

Daniel Ortiz-Barrientos is an Associate Professor in evolutionary genetics in the School of

Biological Sciences at The University of Queensland, Brisbane, Australia. During his scientific
career he has investigated the ecological and genetic basis of speciation both in plants and
animals. His current research program explores the early stages of speciation, the molecular
basis of parallel speciation, and the interplay between recombination and natural selection
during the origin of new species. His research funds come from The Australian Research
Council. He is married to Antonia Posada, and is the father of three energetic and
beautiful kids.

Claudia Russo was born in Leeds, England, but has lived in Rio de Janeiro, Brazil since she
was two years old.
Claudia has an academic major in Ecology from Universidade Federal do Rio de Janeiro
completed in 1989, and finished her Master’s thesis in 1991 on population genetics of two
actiniid species of sea anemones with different reproductive strategies, under the supervision
of Associate Professor Antonio Mateo Sole-Cava. Her PhD dissertation was on the di-
versification of drosophilids and on the use of a known phylogenetic tree to estimate the
reliability of tree building methods. The dissertation was completed in 1995 under the
supervision of the Evan Pugh Professor Masatoshi Nei who recently received the prestigious
Thomas Hunt Morgan Medal. Her graduate degrees were obtained as a student at the
Genetics Program from the Universidade Federal do Rio de Janeiro and as a visiting scholar
at the Pennsylvania State University (1992–1995).
Claudia is currently the Head of the Genetics Department at the Federal University of Rio
de Janeiro, having been a member since 1997. Claudia has supervised 13 Master’s disser-
tations, eight PhD theses and seven post-docs, of which eight are now Assistant Professors at
universities in Brazil and abroad. She has published 42 academic papers that have been cited over 1,200 times. Her h-index is 14.
Since 2012, Claudia has been a member of the editorial board, and an associate editor of the Molecular Biology and Evolution
journal. Since 2012 she has been a council member for the Pan American Association of Computational Interdisciplinary Sciences
and since 2009 for the Brazilian Association for the Advancement of Science.
Claudia’s general academic interests are on key aspects of animal phylogenetics, including their diversification patterns in time
and space. She has worked with various metazoans groups but more prominently on marine sponges, sea anemones, arthropods,
passerine birds, and mammals. Claudia has also published on the use of known phylogenetic trees to estimate the efficiency of
phylogenetic methods in recovering and rooting those trees. More recently, she has developed some interesting hands-on edu-
cational tools for evolutionary biology practices in the classroom.

Karen E. Sears is an evolutionary developmental biologist whose primary research goal is to

determine how developmental variation within a species produces congenital mal-
formations in humans, and among species generates new evolutionary forms in mammals.
Dr. Sears earned her PhD from the University of Chicago, did postdoctoral research at in the
Howard Hughes Medical Institute (HHMI) lab of Dr. Lee Niswander, and joined the faculty
of the University of Illinois at Urbana-Champaign. At Illinois she holds positions as an
Associate Professor in the Department of Animal Biology, a Faculty Member in the Institute
of Genomic Biology, and an Affiliate of the Program in Ecology, Evolution and Conservation
Biology and the Department of Cell and Developmental Biology. She is also the President of
the Pan American Society for Evolutionary Developmental Biology. She has authored or co-
authored over 35 publications including first-authored publications in Nature, Proceedings of
the National Academy of Sciences, and Evolution. She has served as a principal investigator
on multiple, nationally-funded research projects, and presented invited seminars at more
than 30 institutions and symposia. She is routinely ranked among the top 10% of Illinois professors for her teaching, and was a
featured scientist in the PBS/HHMI documentary “Your Inner Fish.”
 Section Editors xi

Vassiliki “Betty” Smocovitis is Professor of the History of Science in the Department of

Biology and in the Department of History at the University of Florida. Her areas of expertise
include the history of evolutionary biology, genetics and systematics and the history of
botany. She is best known for her contributions to understanding the historical event known
as the “evolutionary synthesis” and in gaining greater understanding of the origins of the
discipline of evolutionary biology. She has published extensively on both the intellectual
and social aspects of the history of evolutionary biology including a history of the Society for
the Study of Evolution, a history of the Darwin Centennial of 1959, and the integration of
botany, genetics, and anthropology into the evolutionary synthesis. She was the contributor
to the Oxford Bibliographies entry on Charles Darwin at over 25,000 words and the entry on
the modern synthesis. She is the author of Unifying Biology: The Evolutionary Synthesis and
Evolutionary Biology (Princeton: Princeton University Press, 1996).

Nina Wedell is a professor of evolutionary biology with research interests focused on the
evolutionary ecology of sex. She has worked extensively on various aspects of sexual selec-
tion and sexual conflict, in particular on the role of selfish genetic elements in reproductive
biology. Nina is the Academic lead for the Behaviour research group at the University of
Exeter.

Jason Wolf is Professor of Evolutionary Genetics in the Department of Biology & Bio-
chemistry and The Milner Centre for Evolution at the University of Bath. His research is
unified with a special focus given to understanding the influence that frequently ignored or
under-appreciated sources of genetic variation have on the genotype-phenotype relationship
and how this, in turn, influences evolutionary processes. He integrates theoretical, compu-
tational and empirical quantitative and population genetic techniques to achieve this goal.
He is particularly interested in understanding the evolutionary consequences of various types
of interactions, including gene interactions (epistasis), parent-offspring interactions and
social interactions. He received a PhD from the University of Kentucky, after which he
was a postdoctoral researcher at Indiana University and a US National Science Foundation
Postdoctoral Fellow at Washington University School of Medicine. Prior to moving to the
University of Bath he held positions at the University of Tennessee and the University of
Manchester. He won the Dobzhansky Prize from the Society for the Study of Evolution, a
Young Investigator’s Prize from the American Society of Naturalists and the Scientific Medal
from the Zoological Society of London.
LIST OF CONTRIBUTORS

LT Ackert Jr. DA Baum

Drexel University, Philadelphia, PA, USA University of Wisconsin, Madison, WI, USA
JD Aguirre MS Bergen
Massey University, Auckland, New Zealand Rutgers University, New Brunswick, NJ, USA
RC Albertson M Berger
University of Massachusetts, Amherst, MA, USA Institute of Hygiene, University of Münster, Münster,
AC Algar Germany
University of Nottingham, Nottingham, UK V Berger
RG Allaby Universite ́ Claude Bernard Lyon 1, Villeurbanne, France
University of Warwick, Coventry, UK AJ Betancourt
SH Alonzo Vetmeduni Vienna, Vienna, Austria
University of California, Santa Cruz, CA, USA
LW Beukeboom
L Altenberg University of Groningen, Groningen, The Netherlands
The Konrad Lorenz Institute for Evolution and Cognition
JP Bielawski
Research, Klosterneuburg, Austria
Dalhousie University, Halifax, NS, Canada
DM Althoff
Syracuse University, Syracuse, NY, USA BK Blackman
University of California, Berkeley, CA, USA; and
JM Á lvarez-Castro University of Virginia, Charlottesville, VA, USA
University of Santiago de Compostela, Lugo, Galiza,
Spain H Blackmon
University of Minnesota, Saint Paul, MN, USA
C Amemiya
Benaroya Research Institute, Seattle, WA, USA JL Blois
University of California, Merced, CA, USA
M Ansdell
University of Hawai’i at Mānoa, Honolulu, HI, USA JD Bloom
Fred Hutchinson Cancer Research Center, Seattle, WA,
WS Armbruster USA
University of Portsmouth, Portsmouth, UK
A Blumberg
APA Assis
Ben-Gurion University of the Negev, Beer-Sheva, Israel
Universidade de São Paulo, CEP São Paulo, Brazil
J Blumenstiel
A Aswad
University of Kansas, Lawrence, KS, USA
University of Oxford, Oxford, UK
JR Auld DT Blumstein
West Chester University, West Chester, PA, USA University of California, Los Angeles, CA, USA

CF Baer E Bolund
University of Florida Genetics Institute, Gainesville, FL, Uppsala University, Uppsala, Sweden
USA C Bonenfant
SCH Barrett Universite ́ Claude Bernard Lyon 1, Villeurbanne, France
University of Toronto, Toronto, ON, Canada
S Borish
G Barshad California State University East Bay, Hayward, CA,
Ben-Gurion University of the Negev, Beer-Sheva, Israel USA
J Bast JW Boughman
University of Lausanne, Lausanne, Switzerland Michigan State University, East Lansing, MI, USA

xiii
xiv List of Contributors

BW Bowen BSW Chang

Hawaiʻi Institute of Marine Biology, University of University of Toronto, Toronto, ON, Canada
Hawaiʻi at Mānoa, Kāneʻohe, HI, USA
MA Charleston
LM Boykin University of Tasmania, Hobart, TAS, Australia
The University of Western Australia, Perth, WA,
Australia Q Chen
Rutgers University, New Brunswick, NJ, USA
PLR Brennan
Mount Holyoke College, South Hadley, MA, USA J Chifman
Wake Forest School of Medicine, Winston-Salem, NC,
JC Briggs USA
Oregon State University, Corvallis, OR, USA
P-A Christin
ED Brodie III University of Sheffield, Sheffield, UK
University of Virginia, Charlottesville, VA, USA
JA Clack
TJ Brodribb University Museum of Zoology, Cambridge, UK
University of Tasmania, Hobart, TAS, Australia
FM Cohan
RM Brown Wesleyan University, Middletown, CT, USA
University of Kansas, Lawrence, KS, USA
AA Comeault
LT Buck University of North Carolina, Raleigh, NC, USA
Natural History Museum, London, UK; and University
of Roehampton, Whitelands College, London, UK JK Conner
Michigan State University, Hickory Corners, MI, USA
JG Burleigh
University of Florida, Gainesville, FL, USA BMA Costa
Universidade de São Paulo, CEP São Paulo, Brazil
T Burmester
University of Hamburg, Hamburg, Germany T Coulson
University of Oxford, Oxford, UK
LF Bussier̀ e
University of Stirling, Stirling, UK BA Counterman
Mississippi State University, Mississippi State, MS, USA
R Butlin
University of Sheffield, Sheffield, UK; and University of R Covas
Gothenburg, Strömstad, Sweden CIBIO-InBio, University of Porto, Campus Agraŕ io de
Vairão, Vairão, Portugal
A Caballero
Universidad de Vigo, Vigo, Spain TP Craig
University of Minnesota Duluth, Duluth, MN, USA
RM Calhoun
Western University, London, ON, Canada D Crowson
University of Toronto, Toronto, ON, Canada
U Candolin
University of Helsinki, Helsinki, Finland AD Cutter
University of Toronto, Toronto, ON, Canada
AC Carnaval
The City College of New York, New York, NY, USA; V Daubin
and The Graduate Center of the City University of Centre National de la Recherche Scientifique (CNRS),
New York, New York, NY, USA Universite ́ de Lyon, Villeurbanne, France
A Caro-Quintero PD Polly
University of Texas, Austin, TX, USA Indiana University, Bloomington, IN, USA
RL Carroll FR Davis
Redpath Museum, McGill University, Montreá l, QC, Florida State University, Tallahassee, FL, USA
Canada
GK Davis
F Casey Bryn Mawr College, Bryn Mawr, PA, USA; and The
Park Ave, Merced, CA, USA College of New Jersey, Ewing, NJ, USA
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