Evolutionary genetics, concepts and case studies c fox, j wolf (oxford, 2006) 1

EVOLUTIONARY GENETICS
Concepts and Case Studies


Concepts and Case Studies
AG = G(Y-PP) G + 2M
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Edited by

Charles W. Fox
Jason B. Wolf


Copyrighted mate

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EVOLUTIONARY GENETICS


Copyrighted material
1

*


EVOLUTIONARY GENETICS
Concepts and Case Studies

Edited by
Charles W. Fox
Jason B. Wolf

OXFORD
UNIVERSITY PRESS

2006


OXFORD
Oxford University Press, I n c . publisher works that further
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Evolutionary genets»; concepts and case srudhcVrdited by Oiaries V . Pox, Jason B. Wolf.

p. ion.
Includes bibliographical rrtereiKev
M N - I J 978*0-19-516817-4; 978-CM9-5I6818-1 jpbL)
tSBNO J9 516817 8 ; 0 1 9 5 1 A S I 8 6 (phk.)
L Kvotunonary genetics.
| I ) N I M : L Genetic*, Population. 2- F.volufson. 3, Gcitotypt* 4T M o M s Genetic* 5. Variation (Genetics)
Q H 4SfF.92S 2005) 1. Fox, Charles W. I I . Wolf, Jason K

QH390.E94 2005
572J'3S—dc22

2005011131

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


Preface

E

v o l u t i o n a r y genetics is .1 broad field that has

T h e signature o f this r e v o l u t i o n is clearly seen 111

seen particularly r a p i d g r o w t h and expansion

this v o l u m e , in w h i c h t h e m a j o r i t y o f chapters

in recent years. T h i s diverse field is unified hy a sec

discuss patterns o r processes t h a i occur at t h e

o f m i r r o r -image goals: (1) t o understand the impact

molecular level o r have been influenced by t h e

t h a t e v o l u t i o n a r y processes have o n the patterns o f

availability of molecular d a t a .

genetic v a r i a t i o n w i t h i n and a m o n g p o p u l a t i o n s o r

A l t h o u g h w e m a y define evolutionary genetics

species and (2) t o understand the consequences o f

as a single integrated f i e l d , there is a c o n t i n u u m in

these patterns o f genetic variation l o r various evolu*

t h e degree t o w h i c h research is e v o l u t i o n a r y versus

l i o n a r y processes. Research i n evolutionary genetic*

genetic.

stretches across a c o n t i n u u m o f scale, f r o m studies

informs molecular geneticists, whose primary interest

At one extreme» evolutionary

genetics

o f D N A sequence e v o l u t i o n (e.g.. Chapters 7 and 9i

may he f i n d i n g and characterizing genes affecting

t o studies o f multivariate phenorypic evolution (e.g.,

traits, of the consequences t h a t p o p u l a t i o n suhdivi*

C h a p t e r 2 0 ) , and across a c o n t i n u u m o f rime, f r o m

siou and linkage d i s e q u i l i b r i u m have o n their inter

ancient events that lead t o current species diversity

pretation o f associations between loci and trait

(e.g., Chapter 281 t o r a p i d e v o l u t i o n seen over rela-

expression (e.g., Tcmpleton et aL 2005). At t h e other

tively short t i m e scales in experimental e v o l u t i o n

extreme, evolutionary biologists may use t h e results

studies (Chapter 3 1 ) .

o f these *gene discovery" studies t o identify genes

A major cause o f the recent g r o w t h and e x p a n -

that underlie e v o l u t i o n a r y i m p o r t a n t genetic varia­

t i o n o f evolutionary genetics has been the modern

l i o n (e.g.* Beldade et a l . 2 0 0 2 ) . However, differ»

r e v o l u t i o n in molecular biology, w h i c h has fueled

entitling

research

into

t h e extremes o f

these

the g r o w t h o f areas o f evolutionary genetic* focused

categories is b e c o m i n g increasingly

o n the analysis o f sequence d a t a , the g e n o t y p e -

e v o l u t i o n a r y approaches permeate genetics just as

difficult

as

phenotype relationship, and genome e v o l u t i o n .

molecular biology permeates evolutionary biology.

A l t h o u g h many o f t h e questions at the forefront

T h e development o f this b o o k was i n i t i a t e d

o f the field have been a r o u n d stnee the early days

late in 2 0 0 2 . I t was conceived as a c o m p a n i o n t o

o f evolutionary genetics (e.g., since the M o d e r n

Evolutionary

Ecology:

Concepts

arul CMS*'

Studies

Synthesis), the availability o f relatively inexpensive

(edited by Fox et a l . 2 0 0 1 ) , also published by

h i g h - t h r o u g h put genetic technology and t h e result-

O x f o r d University Press. O u r p r i m a r y objective i n

i n g large databases o f molecular genetic data has led

this b o o k , as in

t o the emergence o f m a n y new areas o f study

provide a c o l l e c t i o n of readings that w i l l i n t r o d u c e

and a sort o f r e v o l u t i o n in e v o l u t i o n a r y genetics,

students t o concepts and c o n t e m p o r a r y

its c o m p a n i o n

v o l u m e , is

to

research


p r o g r a m s in evolutionary genetics. O u r hope w h e n

some o f the research areas and thus discover t h e

conceiving this volume was that it m i g h t be adopted

vast literature t h a t w c have been unable t o include

ai« a text f o r graduate courses and seminars* as ha*

here,

been the case for Evolutionary

Fxology.

We thus

T h e volume is structured i n t o six parts. A l t h o u g h

targeted the level o f this book so that it can be used

this might suggest that there are six clearly defined

by advanced undergraduates, graduate students,

sets o f topics, such structuring is somewhat a r t i f i ­

and established researchers in genetics or e v o l u t i o n

cial. Evolutionary genetics is a highly

integrated

l o o k i n g for a concise i n t r o d u c t i o n t o evolutionary

field w i t h n o clear lines d i v i d i n g research topics.

genetics. Authors were asked t o target this audience

T h e structure o f t h e book is simply a convenient

w h i l e w r i t i n g , and reviewers and t h e editors focused

w a y o f collecting m o r e related topics together. We

on n u k i n g the volume accessible t o this audience

start w i t h a collection o f chapters presenting many

w h i l e reviewing each chapter.

o f the principles o f e v o l u t i o n a r y genetics that serve

Chapter authors are all leading researchers in

as the f o u n d a t i o n for the rest o f the subject (Part I).

their fields and were chosen t o p r o v i d e their partic­

For this part readers need have o n l y a decent back­

ular perspectives on a topic. Chapters thus represent

g r o u n d in genetics, t h o u g h a b a c k g r o u n d in e v o l u ­

the current stage o f evolutionary genetics better than

tionary biology w i l l certainly be helpful. Later parts

any single-authored t e x t b o o k c o u l d , a n d the diver­

o f the book assume an understanding o f b o t h general

sity o f authors introduces readers t o the divcrsiry o f

concepts o f genetics and the concepts presented in

ideas, approaches, and o p i n i o n s t h a t are the nature

earlier p a n s . Parts I W V are ordered hierarchically

o f science. However, a m u l t i - a u t h o r e d

textbook

starting at the basic level o f biological c o m p l e x i t y ,

presents special challenges. A u t h o r s vary in the level

t h e D N A sequence (Part I I ) , b u i l d i n g t h r o u g h devel­

at w h i c h they present material and in the a m o u n t

o p m e n t (Part I I I ) t o studies o f complex phenotypes

o f b a c k g r o u n d that they expect readers t o have.

(quantitative genetics; P a n I V ) and on t o the inter­

Authors also vary in their w r i t i n g styles, t h e w a y

actions between i n d i v i d u a l s and their environment

that they organize their chapters a n d , o f course, each

(sexual and social selection; also Part I V ) . These

has a unique perspective o n the overall field. We

parts are f o l l o w e d by one on the genetics o f species

have attempted t o minimize this v a r i a t i o n t h r o u g h

differences and speciation (Part V ) that integrates

a u t h o r guidelines and by aggressively e d i t i n g and

across the hierarchy o f complexity t o investigate wrhat

revising chapters. H o w e v e r , some variation a m o n g

is often considered the most f u n d a m e n t a l problem

chapters is unavoidable and reflects the variation in

in evolutionary 1 biology: the o r i g i n o f species, l a s t l y

styles and approaches c o m m o n t h r o u g h o u t science.

w c include a part i l l u s t r a t i n g h o w the theoretical,

A s w i t h any b o o k , especially an edited v o l u m e ,

conceptual, and e m p i r i c a l approaches developed in

this book is not comprehensive. T o keep the length

previous chapters are applied t o specific p r o b l e m s

of the book practical, and the price a f f o r d a b l e , w c

in b i o l o g y (Part V I ) . T h e potential choice o f topics

had t o impose restrictions o n chapter length and the

here is e n o r m o u s but w e could choose only a couple

number o f references. T h i s a l l o w e d us t o increase

o f representative examples that w e find particularly

the diversity o f subjects covered but at the expense

exciting,

o f depth o f coverage. M o s t topics could fill an entire

Because w c

enforced length

restrictions

on

book ( a n d m a n y are indeed the subject o f entire

chapters, many i m p o r t a n t and exciting topics were

books). Chapters are intended t o serve as introduc­

necessarily left o u t . O t h e r topics were outside the

tions t o their t o p i c , focusing o n basic concepts

expertise o f t h e authors o r w e r e i m p o r t a n t topics

rather than becoming comprehensive reviews (the

that did not fit well into the structure o f the chapters.

reference l i m i t was intended t o minimize t h e latter).

W c thus include a large number o f boxes focusing

Such a f o r m a t imposed unavoidable l i m i t a t i o n s o n

on specific topics presented largely independently

authors a n d , as e d i t o r s , w e take responsibility for

o f the m a i n body of the text w i t h w h i c h they arc

the necessary omission o f missing topics and the

associated. W i t h the exception o f Box 24.1 { w h i c h

lack o f many a d d i t i o n a l references that are perhaps

w c use t o introduce Part V, Genetics o f Speciation),

equally a p p r o p r i a t e as examples o r case studies.

all boxes appear w i t h i n the pages o f t h e chapters t o

Chapters include a "Suggestions for Further Reading"

w h i c h they arc most relevant. M a n y w r crc w r i t t e n

section t o guide readers o n where t o go next for

by the same author as the chapter that they comple­

a d d i t i o n a l coverage o f t h e topic. We hope that read­

ment; these largely e x p a n d o n topics m e n t i o n e d in

ers w i l l be inspired t o delve m o r e fully i n t o at least

the main body o f t h e chapter o r they present a


topic that did not fit well in the main body of the
chapter Other boxes were written by scientists
who did not write full chapters; these boxes read
more like mini-chapters. Most could indeed have
been full chapters but, alas, the realities of publish­
ing prevented us from including every chapter
we would want* We also included three boxes on
model organisms in biology* (in Pan V!) since so
much of what we know about evolutionary genet*
ics, and biology in general, comes from studies
of model organisms. The choice of box topics reflects
the views of the editors, the reviewers, and the many
chapter authors who suggested topics for boxes.

Lastly, we have compiled a glossary of terms»
Initially wc asked authors to include footnotes or
tables defining the terminology of their Held but the
large number of submissions made this impractical,
so we converted these (at the suggestion of multiple
authors) to a glossary at the end of the text* It is by
no means a comprehensive glossary of genetics or
even evolutionary genetics terms* it is intended to
aid the reader by providing definitions for terms
that might be considered jargon special to some
areas of research, or terms that you know you once
learned but may have since forgoncn; that is, the
terminology not necessarily standard in a working
scientist's vocabulary* The glossary entries are
largely written by the chapter authors, heavily
supplemented (and editcd> by the editors; we have
thus given the appropriate author credit after each
entry. In a few cases we have included multiple
entries for a single term because multiple entries
were submitted by authors and the difference
between those entries was itself informative.
Each chapter and box was reviewed by at least
one other contributor to the book and, in most

cases, one or more external reviewers. Wc are truly
indebted t o all these reviewers for generously
donating their time and providing thorough and
constructive reviews. Without their help it would
nor have been possible t o produce such a volume
given the vast diversity of topics covered and the

limits of the editors* expertise. We thus thank the
external reviewers, including Hiroshi Akashi,
Cerise Allen, Bill Atchlcy, Score Carrol), James Crow,
Mary* Kllen Cze^ak, Tony Frankino, Oscar Ciagginrti,
C. William Kirkpatrick, Larry Leamy, Susan
Lindquist, Curt 1 ivcly, Manyuan )~ong, Bryant
McAllister, Tami Mcndclson, Dchra Murray, Joshua
Mutic, John Obrycki, Susan Perkins, Massimo
Pigliucci, Richard Preziosi, Will Provine, David
Queller, Glenn-Peter Sactre» Laura Salter, Douglas
Schemske, llamish Spencer, Marc Tatar, Kric
(Rick) Taylor, L i n d i Wahi, Cunrcr Wagner,
John Wakeley, Bruce Walsh, Joe Williams, and a
few others who asked to remain anonymous. Wc
also thank Lisa Hitchcock, Denise Johnson, and
Oriaku N j o k u for help proofreading chapter* and
references*
Finally, and most importantly, we thank the
authors for their willingness 10 invest the subsian*
rial amount of time needed t o write excellent chap*
ters and boxes* The success of the volume ultimately
depends on the quality of the contributions by
authors. Wc are fortunate to have recruited an out­
standing group o f scientists who dedicated tremen­
dous time and effort to making this project a success.
Thank you for being such a wonderful group of
people with which t o work!
Charles W. Fox
Jason B* Wolf

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J,


Contents

Conrrihnrnr*

^lll

Part I - Principles of Evolutionary Genetics
1. From Mendel to Molecules: A Brict History of Evolutionary Genetics
Mich.wt

K

i

Motrirf,

2. Genetic Variation
H
Marta L. Wayne and Michael M»
Box 2.1. Maternal Ff frets 19
3 . Mutation
12
David Houle and Alexcy

Miyamoto

Kondrashov

4. Natural Selection £2
Michael /. Wade
Box 4 , 1 . Defining and Measuring Fttnev»
Daphne h Vairbairn

52

V Stochastic Processes in Evolution
til
John H. Cillespie
Box 5,1. The Probability of Extinction of an Allclc
Box 5.2. Mutational Landscape Model 7Q

68

6 . Genetics and Evolution in Structured Populations 8 0
Charles /. Goodnight
Box 6.1. Fpistasis and rhc Conversion ot Generic Variance
Jason B. Wolf

S7

tx

Copyrighted material

Contents

x

Part II - Molecular Evolution

7. Detecting Selection at the Molecular Level
Michael ffi Narhman

103

fl. Rflrr* pf Molecular Bmliitiop LL9
Francisco RodrigueZ'Trelles, Rosa Tarrio and Francisco f. Ayala
Box 8.1, Timing Evolutionary Events with a Molecular Clock 122
Box 8.2. Tjgtjng the Hypothesis of the Molecular Clock 125
9. Weak Selection on Noncoding Gene Features
Ying Chen and Wolfgang Stepban
10. Evolution of Eukaryotic Genome Structure
Dmitri A. Petrov and Jonathan R Wendel

133
144

11. New Genes» New Functions: Gene Family Evolution and Phylogenetics
foe Thornton

157

12. Gene Genealogies 173

Noah A. Rosenberg
Box 12.1. Horizontal Inheritancg

1Z&

Part III - From Genotype to Phenotype
I V C*rnt* F n n r t i n n n n d Mnl**riilar F v n l u r i n n

jJiJ

Simon G I oiagfl
ft**v i i I

I b e Bale ^ Gene Emccactioo M**wnrlfg in Enohitiop

2U0

Stephen R. Proulx
14. Evolution o f M n l r i d o m a i n Protein*

H I

U52/0 Pdtt/JV
15. Evolutionary Developmental Biology

222

Dfliad / Stem
Box 15.2, Functional Assays in Nonmodcl Organisms

229

16. Canalization 215
Mark L* Siegal and Aviv Bergman
Box 16.1. Computational Modeling of the Evolution of Gene Regulatory Networks

17. Evolutionary Epigcnctics 252
Eva fablonka and Marion h Lamb

Part IV - Quantitative Genetics and Selection

18. Evolutionary Quantitative Genetics
Derek A. Roff
ftr»* t f l . l

267

Individual T-irnres SllrfilCa -'"^ Mnlrivariaf^ SckctlQD

lasan B. Wolf

263

243


Contents

XI

19. Genetic Architecture of Quantitative Variation 2X8
fames At. Chevcrud
Box 19.1. Genotvpic Values: Additivitv, Dominance, and Epkrasis
ttox 1 <*.?.. <\mw Valiireand O n r n r Variance 2211
Box 19.3. How to Perform a QTL Analysis 291
Box 19.4. Evolutionary Morphonictrics 294
Christian Peter KlingenberR
Box 19.5. Modularity 304
lason G. Mezev
2 0 . Fvnhirion of Genetic Variance-Covariance Structure
Patrick C. Phillips and Katrina L. McGtagan
Box 20.1. What U .i Co-variance? 311
Box 20-2. Plciotropic Effects 313
Box 20.3. Evolution of the G Matrix 316
2 1 . Genotype-Environment Interactions and Evolution
Samuel At. Srhriner

289

UH

326

2 2 . GenCtka of Sexual Selection
119
Allen /. Moore j«rf Patricia /. M o o r e
Stwpn A. Frank
Box 2 3 X Coefficients of Relatedness

352

Part V - Genetics of Speciation
Box, Species Concepts
lames Mallrt

367

24. The Evolution of Reproductive Isolating Barriers
Norman A. Johnson

374

2 5 . Genetics of Reproductive Isolation and Species Differences in Model Organisms
Pawel Michalak and Mohamed A. F Nnor
Box 25.1. The Dohzhanskv-Mullcr Model 392
2 6 . Natural Hybridization
399
Michael I.. Arnold and John At. Burke
Box 26.1. Porential Outcomes of Natural Hybridization

387

400

2 7 . Population Bottlenecks and Founder Effects
414
Lisa Marie Meffert
Box 27. L Models of the Shifts in Selection Pressures Experienced by Bottlcnecked
Populations 415
2 8 . Theory of Phylogcnetic Estimation

426
T
Asblev \ . F.gan and Keith A. Crandall
Box 28.1. Philosophical ;uui Methodological Diffcrcnccs in Phylofienetics

434

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XH

Contents
Part VI - Evolutionary Genetics in Action

29. Evolutionary Genetics of Host-Parasite Interactions

447

Box 29,1, The CBox 29,2, Arahtdopsis as a Model Organism in Evolutionary Genetics 453
Kcntaro K. Shimizu ami Michael D. Puni^anan
Box 29,3. Evolution of Virulence 456
30. The Evolutionary Genetics of Senescence 464
Daniel £ . /.. Vromishw and Anne M.
Rronikowski
Box 30*1. Demography of an Age-Structured Population 466
Box 30.2. Drosophifo as g Model Organism in Evolutionary Biology
Jeffrey R. Powell
3 1 . Experimental Evolution 482

Adam K> Chippindale
Box 31.1. E, colt as a Model Organism in Evolutionary Genetics
Richard E. Lcnski
32. Evolutionary Conservation Genetics
Richard
trankham
Glossary

Refcances

513

^7

502

485

471


Contrii

Michael L. Arnold
Department of Genetics
University of Georgia
Athens, Georgia 30602, USA

James M. Chcvcrud
Department of Anatomy and Neurohiology

Washington University School of Medicine
St. Louis, Missouri 6.1110, USA

Francisco J. Ayala
Department of Ecology and Evolution
University of California
Irvine, California 92697, USA

Adam K. Chippindale
Department of Biology
Queen's University
Kingston, Ontario K7L 3N6, Canada

Aviv Bergman
Department of Pathology and
Molecular Genetics
Albert Einstein College of Medicine
New York, New York 10461, USA

Keith A. Crandall
Department of Microbiology and
Molecular Biology
Brigham Young University
Prove, Utah 84602, USA

Anne M. Bronikowski
Department of Ecology
Evolution and Organtsmal Biology
Iowa State University
Ames, Iowa 50011, USA

Michael R. Dietrich
Department of Biological Sciences
Dartmouth College
Hanover, New Hampshire 03755, USA

John Mi Burke
Department of Biological Sciences
Vandcrbilt University
Nashville, Tennessee 37235, USA

Ashley N. Egan
Department of Microbiology and
Molecular Biology
Brigham Young University
Provo, Utah 84602, USA'

Ying Chen
Department of Ecology and Evolution
University of Chicago
Chicago, Illinois 60637, USA

Daphne J. Fairbairn
Department of Biology
University of California
Riverside, California 92521, USA
Kill

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I

Kiv

Steven A. Frank
Department of Ecology and Evolutionary
Biology
University of California
Irvine, California 92697, USA
Richard Frankham
Department of Biological Sciences
Macquarie University
NSW 2109, Australia
John H. Gillcspic
9849 Martingham Circle
St. Michaels, Maryland 21663, USA
Charles J. Goodnight
Department of Biology
University of Vermont
Burlington, Vermont 054065, USA
David Houle
Department of Biological Science
Florida State University
Tallahassee, Florida 32306, USA
Eva Jablonka
The Cohn Institute for the History and
Philosophy of Science and Ideas
Tel Aviv University
Tel Aviv 69789, Israel

Norman A-Johnson
Department of Kntomology
Program in Organismic Biology and
Evolution
University of Massachusetts
Amherst, Massachusetts 01003, USA
Christian Peter Klingcnberg
Faculty of Life Sciences
University of Manchester
Manchester M13 9PT, United Kingdom
Alcxey Kondrashov
National Center for Biotechnology
Information
National Institutes of Health
Bethesda, Maryland 20894, USA

Contributors
Paula X. Kover
Faculty of Life Sciences
University of Manchester
Manchester M13 9PT, United Kingdom
Marion J. Lamb
Senior Lecturer (retired!
Birkbeck College
University of London, United Kingdom
Richard E. Lcnski
Department of Microbiology and Molecular
Genetics
Michigan State University
East Lansing, Michigan 48824, USA

Simon C Lovcll
Faculty of Life Sciences
University of Manchester
Manchester M I 3 9PT, United Kingdom
James Mallet
Department of Biology
University College London
London NW1 2HE, United Kingdom
Katrina L. McGuigan
Center for Ecology and Evolutionary Biology
University of Oregon
Eugene, Oregon 97405, USA
Lisa M. Meffert
Department of Ecology and Evolutionary
Biology
Rice University
Houston, Texas 77251, USA
Jason G. Mezey
Department of Biological Statistics and
Computational Biology
Cornell University7
Ithaca, New York 14853, USA
Pawcl Michalak
Department of Biology
University of Texas
Arlington, Texas 76019-0498, USA

Copyrighted mater:

Contributors
Michael M. Miyamoto
Department of Zoology
University of Florida
Gainesville, Florida 32611, USA

Jeffrey R. Powell
Department of Ecology and Evolutionary

Biology
Yale University
New Haven, Connecticut 06520, USA

Allen J. Moore
Centre for Ecology and Conservation
University of Exeter in Cornwall
Tremough, Pcnryn TRIO 9EZ,
United Kingdom

Daniel E. L. PromUlow
Department of Genetics
The University of Georgia
Athens, Georgia 30602» USA

Patricia J. Moore
Centre for Ecology and Conservation
University of Exeter in Cornwall
Tremough, Pcnryn TRIO 9EZ»
United Kingdom

Stephen Proulx
Department of Ecology, Evolution and
Organismal Biology
University of Iowa
Ames, Iowa 50011, USA.

Timothy A. Mousscau
Department of Biological Sciences
University of South Carolina
Columbia, South Carolina 29208, USA

Michael D. Purugganan
Department of Genetics
North Carolina State University
Raleigh, North Carolina 27695, USA

Michael W. Nachman
Department of Ecology and Evolutionary
Biology
University of Arizona
Tucson» Arizona 85721» USA

Francisco Rodrigucz-Trellcs
Fundacion Puhlica dc Medieina Genomica
Hospital Clinico Universirario
Universidad de Santiago de Composrela
15706 Santiago. Spain

Mohamcd A* F. Noor
DCMB Croup/Biology

Duke University
Durham, North Carolina 27708, USA

Derek A, Roff
Department of Biology
University of California
Riverside, California 92521» USA

Laszlo Patthy
Institute of Enzymology
Biological Research Center
Hungarian Academy of Sciences
Budapest H-1518, Hungary

Noah A. Rosenberg
Department of Human Genetics and
Bioinformatics Program
University of Michigan
Ann Arbor, Michigan 48109-2218, USA

Dmitri A. Petrov
Department of Biological Sciences
Stanford University
Stanford, California 94305, USA

Samuel M. Scheiner
Division of Environmental Biology
National Science Foundation
Arlington, Virginia 22230, USA

Patrick C- Phillips
Center for Ecology and Evolutionary Biology
University of Oregon
Eugene» Oregon 97405, USA

Kcntaro K. Shimizu
Department of Genetics
Box 7614
North Carolina State University
Raleigh» North Carolina 27695, USA

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xvi

Contributors

Mark L, Sjggaj
Department of Biology
New York University
New York. New York 10003, USA

Wolfgang Stcphan
Department of Biology II
University of Munich
Gmsshadcnm Strasac 2
82152 Plancgg-Martinsried, Germany
David L. Stern
Department of Ecology and Evolutionary

Biology
Princeton University
Princeton, New Jersey 08544, USA
Rosa Tarno
Fundacion Publica de Medicina Genomica
Hospital Clinico Universitario
Universidad dc Santiago de Compostcla
15706 Santiago, Spain
Joseph U. Thornton
Center for Ecology and Evolutionary Biology
University of Oregon
Eugene, Oregon 97403. USA

Michael J. V^ade
Department of Biology
Indiana University
Bloomington. Indiana 47405, USA
Marta L. Wayne
Department of Zoology
University of Florida
Gainesville. Florida 32611, USA
Jonathan F. Wendd
Department of Botany
Iowa State University
Ames, Iowa 5001. USA
Jason B. Wolf
Faculty of Life Sciences
University of Manchester
Manchester, M l 3 9PT, United Kingdom

PRINCIPLES OF EVOLUTIONARY GENETICS

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I

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1
From Mendel to Molecules: A Brief History
of Evolutionary Genetics
MICHAEL R. DIETRICH

iologists have been g r a p p l i n g w i t h selection ever

B

such as the use o f c h r o m o s o m a l inversions, elec-

selection—not natural selection» but the selection

since D a r w i n . Historians also face a problem o f

r r o p h o r e s i s , sequence data»

c o m p u t e r simulations, and t h e vast array o f e v o l u ­

of w h i c h events t o include i n their narratives* N o

tionary models and concepts ( L e w o n t i n 1 9 8 1 , 1 9 9 1 ;

historical narrative c a n be complete i n the sense o f

Kohlcr 1 9 9 1 ; Powell 1 9 9 4 ; G a y o n & Veuille 2 0 0 1 ) .

population

cages,

including every event, actor, and idea. H i s t o r i a n s

In this brief history; I w i l l focus o n the major

must choose w h i c h events they w i l l include and

controversies that have m a r k e d the historv o f cvolu-

w h i c h they w i l l n o t . W r i t i n g a survey o f the history

tionary

of evolutionary genetics in such a short space makes

emphasis o n the nature of genetic variability and the

this problem o f selection especially acute.

evolutionary processes acting upon this variability*

genetics in the twentieth century w i t h special

A number o f different approaches have been

This approach captures key developments in e v o l u ­

taken t o the history o f evolutionary genetics* W i l l

tionary genetics such as the resolution of the conflict

Provine has suggested that the history o f evolutionary

between Mendelism and D a r w i n i s m and t h e c o n t i n *

biology is one o f persistent controversy* (Provine

uing i m p a c t of molecular biology and molecular

1989; see also L e w o n t i n 1974). Certainly one c o u l d

techniques*

w r i t e a h i s t o r y o f e v o l u t i o n a r y genetics in terms o f
(he disputes between, for instance, the Mcndehans
and Biomctricians, Sewall W r i g h t a n d R. A . Fisher,

MENDEUANS. DARWINIANS.

saltationists and gradualists, the classical and balance

A N D T H E ORIGINS OF

approaches, and neutralists and selectionists (Provine

EVOLUTIONARY GENETICS

1 9 8 6 , 1 9 9 0 ; Beany 1 9 8 7 b ; D i e t r i c h 1 9 9 4 , 199S,
1 9 9 8 ; Smocovitis 1 9 9 6 ; Skipper 2 0 0 2 ) . Such a n

T h e study of evolution and heredity have been inter­

antagonistic view o f evolutionary genetics comple­

t w i n e d since at least Grcgor Mendel's and Charles

ments histories emphasizing the great collaborations

Darwin's separate efforts t o make sense o f the origins

that h a w also characterized the history o f the subject,

o f varieties and the stability of species* Mendel's

such as those between Theodosius

Dobzhansky

experiments w i t h m a n y different species sought l o

and Sewall W r i g h t , E- B. F o r d and R. A . Fisher, o r

explore t h e idea t h a t new stable varieties could

indeed those w i t h i n any o f the m a n y laboratory

be created t h r o u g h h y b r i d i z a t i o n ( O l b y 1979). H i s

groups w o r k i n g in the t w e n t i e t h century (Provine

f a m o u s series o f experiments w i t h the garden pea

19861, M o r e institutionally m i n d e d historians have

quantified the instability o f his h y b r i d crosses as ir

emphasized the rise o f societies, j o u r n a l s , and f u n d ­

documented their hereditary patterns. Darwin's much

ing sources (Smocovitis 1996; C a i n 1993)* A t the

less q u a n t i t a t i v e approach t o hereditary stability

same time, others have documented the development

o r c o n t i n u i t y across generations put much greater

of theoretical a m i experimental tools and techniques,

emphasis o n processes <>r evolutionary change and

3

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4

Principles of Evolutionary Genetics

the problem of the origin of heritable variation.
The differences between Mendel and Darwin were
exaggerated after the rediscovery of Mendel's work
in 1900 hy Carl Corrcns, Hugo Dc Vrics, and Erich
von Tsehcrmak. At this nmc, Darwinian evolution
was criticized as insufficient for the production
of new species (Bowler 1983). Evolution was widely
acknowledged, but the processes of evolution
remained in dispute. Hugo De Vrics, for instance,
articulated his Mutation Theory as a saltarionist
alternative to Darwinism during this period. Even
Darwin's early defenders expressed concern about
Darwin's account of the power of natural selection
(Provine 1971).
Darwin acknowledged two forms of variation:
continuous or blending variations and "sports* or
monstrosities. Although he admincd that his knowl­
edge of variation was insufficient, Darwin thought

that continuous variations were the source of heri­
table variation for natural selection. "Sports'* were
larger* structural deviations, which Darwin thought
were too rare and too harmful t o be of evolution­
ary significance. Fleming Jenkins criticisms of his
views in the Origin of Species caused Darwin to
take the idea of "sports* or discontinuous varia­
tion more seriously. Although "Darwin's bulldog,"
T, H, Huxley, advocated discontinuous variation,
advocacy of this view is often associated with
the early Mendelians, Hugo Dc Vrics and William
Bateson (Provine 1971; Kim 1994).
Darwin developed his own theory of blending
inheritance as a physiological theory called "pangcncsis," Like other material theories of heredity that
would follow Darwin's in the late nineteenth century,
Darwin postulated hereditary particles, pangenes,
which corresponded t o different body parts and
were collected and transmitted via the gametes*
While Darwin's cousin, Francis Galton, helped to
refute this theory, he supported blending inheritance
by developing statistical tools for precisely describ­
ing the similarities between characters. Using corre­
lation and regression, Galton reconsidered heredity
from a statistical point of view. Because he under*
stood characters t o he continuous, Galton believed
that their distribution was best described hy a normal
distribution. The effects o f selection were reconsid­
ered in terms of effects on population means and
variances. Selection could shift the mean of a popu­
lation over a number of generations to create a new

characteristic population mean. The relationship
between parent and offspring was presented in terms

of a law* of ancestral heredity where a particular
character of an offspring CM he determined from
the diminishing contribution of its ancestors I Provine
1971; Kim 1994). Galton's Natural
Inheritance
(1889) inspired Karl Pearson and \V. K R. Weldon
to develop a statistical approach to biology and
evolution that they called biometrics. Within the
biomctrical tradition, weldon and others applied
statistical methods to support gradual Darwinian
evolution by natural selection. Weldon himself
collected statistical evidence from crab carapaces,
which he thought demonstrated the effect of selec­
tion in reducing population variability as well as the
size of the carapace front. These and other efforts
convinced the Biometricians that statistical methods
were essential for understanding evolution and
heredity.
William Bateson had also been impressed
with Gallon's work, hut was not convinced that
statistical methods were the best tools or that either
evolution or heredity should be understood as
continuous or blending. In 1894, Bateson argued in
his book. Materials for the Study of Variation tvith
Special Regard to Discontinuity in the Origin of
Species, that discontinuous variations were common
and saltational evolution of new species was prob­

ably the norm. The dispute between Bateson and the
Biometricians began with Weldon's hostile review of
his book. It was transformed into the MendelianBiometrician controversy when Bateson read
Mendel's paper in 1900. Bateson translated Mendel's
paper into English and immediately began champi­
oning it as the key to heredity and evolution» As a
result» Weldon and Pearson would debate the
significance of Mendel's paper vociferously over
the next 10 years*
The dispute between the Mendelians and
Biometricians was at once about genetic variation
(continuous vs. discontinuous) and evolutionary
change (gradual vs. saltational) as well as the appro­
priateness of statistical methods, and was overlaid
with a struggle for authority and position within
English biology. During the course of this dispute,
the Biometricians and Mendelians drew on extended
networks of biologists, and historian Kyung-Man
Kim argues that the controversy was resolved by
members of this extended network, not by the prin­
cipal antagonists who remained strongly polarized
4Kim 1994). A. D. Darbishirc, for instance, set out to
refute Mendelism with a set of experiments on albino
and waltzing mice. Following Galton, Darbishirc


From Mendel t o Molecules

S

that as the p r o p o r t i o n o f albino mice

THE DEVELOPMENT OF

f o r m i n g the parental and grandparcnral genera­

POPULATION CENETICS

reasoned

tions increased s o should t h e percentage o f a l b i n o
offspring i D a r b i s h i r e 1904). Darbishire's evidence

Regardless o f

in 1904 seemed t o support exactly this interpretation

Biometrician controversy, the use ot statistical meth­

until both W i l l i a m Castle and W i l l i a m Bateson wrote

ods f o r m a l i z e d a p o p u l a t i o n approach t o e v o l u t i o n

devastating critiques

the

Mendelian-

Darbishirc's

in ihc early Twentieth century. A t a t i m e w h e n even

results in Mcndciian terms (Castle 190.5; K i m 1994).

ihe basic language o f gencocs had yet t o be standard­

l>arbjshirc himself was convinced w h e n he tested

ized. it is not surprising that different approaches

his hybrids and realized that some of the mice that

t o the mathematical description o f e v o l u t i o n w o u l d

produced only a l b i n o offspring d i d so because they

also arise. T h e rise of mathematical

were d o m i n a n t . In this case, statistical analysis o f

genetics is usually associated w i t h the w o r k o f three

external appearance was not a reliable guide t o

founders: Sewall W r i g h t , R. A . Fisher, and J. B. S.

genetic constitution* Darbishire's defection infuriated

Haldane. Their w o r k set the foundations for popula­

Pearson* but this was one o f several conversions

tion genetics, as each attempted t o formally reconcile

I K i m 1994).

Mendelism and D a r w i n i s m (Provine 1971).

More

reinterpreting

the outcome o f

after

W r i g h t was an American biologist trained i n

line

genetics at H a r v a r d University by W i l l i a m Castle.

approach. Beginning in 1 9 0 1 , Johannsen sought t o

H i s early interest in m a m m a l i a n genetics led h i m t o

rest whether selection c o u l d change the mean o f a

create t h e m e t h o d o f path analysis as a staff scien­

Wilhelm

biologists joined the Mendelians

population

Johannscn

introduced

his

pure

population's character distribution. Using a continu­

tist at the US Department o f Agriculture. By 1 9 2 1 ,

ous d i s t r i b u t i o n o f bean size and w e i g h t , Johannsen

he had developed his m e t h o d o f path coefficients

selected f o r large, medium» and small beans. H e

t o describe the effects o f inbreeding, assortativc

discovered that after many generations o f selection

m a t i n g , and selection. W h e n he joined the faculty

he could isolate a number o f pure lines from the

o f the University of C Chicago in 1923, W r i g h t shifted

original d i s t r i b u t i o n , Pure lines had stable characters

hts thoughts f r o m guinea pig colonies and cattle

and selection n o longer had an effect on their i n d i ­

herds t o e v o l v i n g natural populations. By 1 9 3 1 *

vidual means. Selection had made a difference in the

he had articulated his shifting balance theory of

original p o p u l a t i o n because it was selecting a m o n g

e v o l u t i o n in his n o w classic paper " E v o l u t i o n in

different pure lines, n o t because it was selecting

M e n d e l i a n Populations'' ( W r i g h t

w i t h i n a pure line. Johannsen's d i s t i n c t i o n between

1986).

the d i s t r i b u t i o n o f a character ( p h c n o t y p e l and the

underlying pure line (genotype) was essential for

1 9 3 1 ; Provine

R. A . Fisher was an Fnglish biologist trained
at C a m b r i d g e

in

mathematics.

Introduced

to

resolving the M e n d e l i a n - B i o m e t r i c i a n controversy*

Mendelism and Biometry at C a m b r i d g e ,

As early as 1 9 0 4 , English mathematician G. U d n y

sought l o reconcile the t w o by understanding the

Fisher

Yute rccogniwd this as a way t o reconcile the hiomcr-

b i o m c i r i c a l properties of M e n d e l i a n populations.

rical description

T h i s approach led h i m t o characterize similarities

of phenorypes w i t h

Mendehan

descriptions o f genotypes. This r o u t e t o reconcilia­

w i t h i n Mendelian populations in terms of their vari­

t i o n was reinforced w i t h evidence f o r

multiple

ance and the contributions t o variance f r o m genetic

factors, w h i c h a l l o w e d Mendelians t o e x p l a i n a

sources, environmental sources, dominance, and gene

continuous character d i s t r i b u t i o n as the result o f

interactions. Fisher\ approach emphasized natural

the interaction o f m a n y genes, each o f small effect*

selection acting in very large n a t u r a l populations.

By 1 9 1 0 , these developments had begun t o signifi­

H e set out his general theory i n his 1930 b o o k . The

cantly depolarize this controversy as many biologist

GcnctWixl

recognized the c o m p a t i b i l i t y o f the M c n d e l i a n and

1971. I9S6L

b i o m c i r i c a l approaches ( K i m 1994), 1

Theory

of

Natural

Selection

I Provine

J. B. S. Haldane was also an raiglish biologist
w i t h b r o a d interests. H e studied mathematics at
O x f o r d before switching t o classics and philosophy.

^Hitlufv^il niterprciatHint of thitiriiiiiftti'rrti h-nr ihcmtrkc*
Iven the 4uhvrxf ■>* o»nirmtm ttKicrrning the rebmc ro*c> ot
etkJrnU' and *uCiM i*nnr* in «he emirte «>f thr ditpint. Src Kim

Beginning in 1922, Haldane sought t o analyze the
mathematical consequences o t natural selection,
Starting f r o m simple Mendehan models using t w o

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6

Principles o f Evolutionary Genetics

allelesat a single locus* Haldane went on t o consider

has resurfaced in recent years w i t h new protago­

selection w i t h self-fertilization, i n b r e e d i n g , over­

nists (Skipper 2 0 0 2 ) , but t h e o r i g i n a l debate was

lapping generations* incomplete dominance, isola­

especially influential because it occurred just as

t i o n , m i g r a t i o n , and fluctuating selection intensities

N e o - D a r w i n i s m was being articulated in the evolu­

(Provinc 1971). Haldanc's scries o f nine papers o n

tionary synthesis (Provine 1992)*

selection c u l m i n a t e d in his 1932 book* The Causes
of Evolution.

In the appendix t o this b o o k , Haldane

compares his views t o those o f Fisher and W r i g h t ,

THE EVOLUTIONARY

While he agrees w i t h elements o f b o t h o f their views,

SYNTHESIS

Haldane differed f r o m Fisher by placing greater
emphasis o n s t r o n g selection o f single genes, migra­

The evolutionary synthesis is identified by historians

t i o n , and cpisrasis. H e sided w i t h Fisher, however,

w i t h both the emerging discipline o f evolutionary

in t h i n k i n g t h a i W r i g h t put t o o much emphasis o n

biology and the integration of previously divergent

random generic d r i f t (Provine 1 9 7 1 ; Oillespie, C h . S

fields such as paleontology, zoology, botany, systcm-

of this volume),

atics, and genetics. According t o this interpretation,

W h i l e Fisher, W r i g h t , and Haldanc approached

the synthesis refers t o a time beginning in t h e 1930s

evolution and p o p u l a t i o n genetics f r o m different

when a range of arguments were offered t o show that

mathematical perspectives, their disagreements were

different fields relevant t o e v o l u t i o n were in fact

not about mathematics, but a b o u t

evolutionary

compatible w i t h each other. These c o m p a t i b i l i t y

processes and concepts and their representation in

arguments helped spur on the emergence o f e v o l u ­

different mathematical models. A c c o r d i n g t o W i l l

tionary b i o l o g y as a field o f i n q u i r y — a s a new a n d

Provine, Fisher and W r i g h t were engaged in a series

centrally i m p o r t a n t discipline (Smocovitis 1 9 9 6 ) .

o f disputes f r o m 1929 u n t i l 1962 when Fisher died

C o m p a t i b i l i t y arguments d o not necessarily i m p l y

(Provine 1 9 8 6 , 1992)- W h i l e they debated many

that there was widespread agreement on a new*

things, the core o f their difference lay in their general

synthetic theory o f e v o l u t i o n . A s Provinc and others

theories o f e v o l u t i o n : Wright's shifting

balance

have argued, there was little agreement a b o u t the

rhcory and Fisher's large p o p u l a t i o n theory, Wright's

mechanisms o f e v o l u t i o n d u r i n g the 1930s and

approach i n c o r p o r a t e d an array o f e v o l u t i o n a r y

1940s, Instead Provine suggests that w c reconsider

processes and emphasized p o p u l a t i o n subdivision

this p e r i o d as a n evolutionary

( G o o d n i g h t , C h . 6 o f this v o l u m e ) . Fisher argued

vast c u t - d o w n o f the variables considered i m p o r t a n t

that n a t u r a l selection was the d o m i n a n t

t o t h e e v o l u t i o n a r y process,** A c c o r d i n g t o P r o v i n c ,

process

and that large populations were the o p t i m u m . These

"Tlic

differences were most apparent a r o u n d the issue o f

understand t h a t evolutionists after

the relative importance o f r a n d o m genetic d r i f t .

disagree intensely w i t h each other a b o u t effective

A l t h o u g h W r i g h t c o n t i n u e d t o elaborate his view's,

population

his early w o r k on the shifting balance rhcory gave

genetic d r i f t , levels o f hcrcrozygosiry,

random drift

rates, m i g r a t i o n rates, e t c , but all c o u l d agree t h a t

a considerable role in evolution,

term

'evolutionary

constriction—**a

constriction* helps

size, p o p u l a t i o n

1930

structure,

random
mutation

T o counter Wright's view, Fisher and his colleague

these variables were o r c o u l d be i m p o r t a n t

E, B. Ford studied yearly fluctuations in the gene

e v o l u t i o n in nature, and that purposive

(allelc) frequencies o f the m o t h Panaxia

played n o role at a l l " (Provine 19881,

dommula

from 1941 t o 1946. They f o u n d that the fluctua­
tions they observed were t o o great t o be accounted
f o r by t h e a c t i o n o f r a n d o m genetic d r i f t . Instead,
they proposed t h a t the

fluctuations

w e r e the result

o f r a n d o m fluctuations i n the strength o f n a t u r a l
selection. As this dispute intensified and extended
i n t h e 1950s t o results o n b a n d i n g patterns i n t h e
snail Cepaea rtemorali$t

W r i g h t began t o m o d i f y

hts views, l i m i t i n g the action of random d r i f t t o large,

but subdivided populations where it could serve as a
means f o r generating novel genotypic combinations
(Provine 1986, 1992), T h e W r i g h t - F i s h e r debate

us

might

in

forces

The foundation for the evolutionary synthesis
was communicated in a number of now classic texts:
R. A. Fisher's The Genetical Theory of Natural
Selection (1930), Thcodosius Dohzhansky's Genetics
and the Origins of Species (1937), Julian Huxley's
Evolution: The Modern Synthesis (1942), Ernst
Mayr's Systematic* and the Origin of Species (1942),
G. G. Simpson's Tempo and Mode in Evolution
(1944), and G. L. Stebbins* Variation and Evolution
m Plants (1950).
Dobzhansky's w o r k

represented the state o f

the art in animal genetics a n d p o p u l a t i o n genetics.