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Sex Allocation

Sex Allocation

by Stuart WestStuart West


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Recent decades have witnessed an explosion of theoretical and empirical studies of sex allocation, transforming how we understand the allocation of resources to male and female reproduction in vertebrates, invertebrates, protozoa, and plants. In this landmark book, Stuart West synthesizes the vast literature on sex allocation, providing the conceptual framework the field has been lacking and demonstrating how sex-allocation studies can shed light on broader questions in evolutionary and behavioral biology.

West clarifies fundamental misconceptions in the application of theory to empirical data. He examines the field's successes and failures, and describes the research areas where much important work is yet to be done. West reveals how a shared underlying theoretical framework unites findings of sex-ratio variation across a huge range of life forms, from malarial parasites and hermaphroditic worms to sex-changing fish and mammals. He shows how research on sex allocation has been central to many critical questions and controversies in evolutionary and behavioral biology, and he argues that sex-allocation research serves as a key testing ground for different theoretical approaches and can help resolve debates about social evolution, parent-offspring conflict, genomic conflict, and levels of selection.

Certain to become the defining book on the subject for the next generation of researchers, Sex Allocation explains why the study of sex allocation provides an ideal model system for advancing our understanding of the constraints on adaptation among all living things in the natural world.

Product Details

ISBN-13: 9780691089645
Publisher: Princeton University Press
Publication date: 10/18/2009
Series: Monographs in Population Biology , #44
Edition description: New Edition
Pages: 480
Product dimensions: 6.00(w) x 9.20(h) x 1.40(d)

About the Author

Stuart West is professor of evolutionary biology at the University of Oxford.

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Sex Allocation



Copyright © 2009 Princeton University Press
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ISBN: 978-0-691-08964-5

Chapter One

Sex Allocation

I would regard the problem of sex ratio as solved (see pp. 146-156). -Williams 1966, p. 272

In this chapter, I describe my reasons for writing this book. In order to provide some context, I start by presenting the problems of sex allocation and a short, potted history of the field. I then provide a discussion of why I hope this book will prove useful, a description of the book contents, and tips on how to read it.


Sex allocation is the allocation of resources to male versus female reproduction in sexual species (Charnov 1979c, 1982). Sex allocation depends on the breeding system of a species, as well as on how reproduction is carried out within each breeding system. Breeding systems can be categorized as dioecious, in which individuals are either male or female for their entire lifetime (e.g., birds and mammals), or hermaphroditic, in which the same individual can produce both male and female gametes. Hermaphrodites can be either sequential or simultaneous. Sequential hermaphrodites, or sex changers, function as one sex early in their life and then switch to the other (e.g., some reef fish such as angelfish and some invertebrates such as Pandalid shrimps). Simultaneous hermaphrodites are capable of both female and male reproduction at the same time (e.g., most flowering plants).

Given the preceding scheme, the six fundamental problems of sex allocation are as follows (Charnov 1979c, 1982):

Under what conditions are sequential hermaphroditism, simultaneous hermaphroditism, or dioecy evolutionarily stable (ES)? When is a mixture of sexual types stable, such as in gynodioecious plant populations, which contain both simultaneous hermaphrodites and females?

For a dioecious species, should the sex of the offspring be determined by the mother, the environment (environmental sex determination), or randomly (chromosomal sex determination)?

Given dioecy, what is the ES offspring sex ratio to produce, defined as the proportion of males in a brood?

For a sequential hermaphrodite, what is the ES sex order (male or female first) and time of sex change?

For a simultaneous hermaphrodite, what is the equilibrium allocation of resources to male and female reproduction?

For all breeding systems, when does selection favor the ability of an individual to alter its allocation to male versus female function in response to particular environmental conditions?


In this section, I give a brief and oversimplified history of the development of the field of sex allocation. I divide the history into pre- and post-Charnov's (1982) monograph, as most historical accounts usually cover only up to 1982.

1.2.1 Pre-Charnov

Darwin (1871, 1874) realized that the preponderance of unbiased sex ratios posed a problem for his theory of natural selection. He made a start at developing possible explanations but was unsatisfied and left the problem for future generations (see section 2.3). This problem was solved decisively by Fisher (1930), who showed that selection for an unbiased sex ratio follows from the fact that each offspring has a mother and father, and so males and females make equal genetic contributions to the next generation (section 2.2). Importantly, Fisher clarified the frequency-dependent nature of selection on sex allocation that is at the center of all subsequent developments.

Modern research on sex allocation began with Hamilton (1967), who made five pivotal contributions to the field of sex allocation and to evolutionary biology more generally. First, Hamilton showed how competition between relatives can select for biased sex allocation. When populations are structured such that brothers compete for mates, this leads to selection for a female biased sex allocation by a process that Hamilton termed local mate competition (LMC). This insight has led to one of the most productive areas of evolutionary biology (chapters 3 to 5). Second, Hamilton showed how the sex ratio can be modeled using game theory. His approach for determining the "unbeatable strategy" was very similar to and laid the foundation for the technically superior evolutionary stable strategy (ESS) approach that was later formalized by Maynard Smith and Price (1973). Third, he showed that simple mathematical models could be used to make comparative predictions that could be easily tested (section His specific example was to show that selection favors more female biased sex ratios when less females lay eggs on a patch and that this could be tested either by comparing across species or by looking at how individuals vary their behavior under different conditions (chapter 4). The use of comparative predictions is taken for granted today because these predictions form the daily bread of evolutionary and behavioral ecology research programs. However, it should be remembered just how astounding this was at the time, to suggest that a few lines of simple maths could make testable predictions about how organisms should behave (Frank 2002). Fourth, he showed how different genes within a genome can be selected to pursue their own selfish interests, to the detriment of other members of the genome, and the way in which meiotic drive fitted into this framework. Fifth, by emphasizing the costliness of male production and the evolution of parthenogenesis, he helped to initiate the debate over the adaptive function of sex (Hamilton 1996).

The next major step was made by Trivers and Willard (1973), who showed that individuals could be selected to adjust the sex of their offspring in response to environmental conditions. They discussed their prediction in the context of mammals such as caribou, and why offspring sex ratios might be adjusted in response to maternal condition. Charnov and colleagues built upon this work by showing how the same principle could be applied more widely to a huge range of issues in both dioecious and hermaphroditic species (chapters 6 and 7)-for example, whether host size should influence offspring sex ratios in parasitoid wasps, the age and direction of sex change in sequential hermaphrodites, and when different breeding systems such as simultaneous hermaphroditism or environmental sex determination (ESD) should be favored (Warner et al. 1975; Charnov et al. 1976; Leigh et al. 1976; Charnov and Bull 1977; Charnov et al. 1978; Charnov 1979c; Charnov et al. 1981; Charnov 1982). Importantly, these predictions clearly lend themselves to empirical testing, which has helped make the Trivers and Willard hypothesis and its various extensions one of the two most productive areas of sex allocation, alongside LMC theory.

Another major strand of sex allocation research was initiated when Trivers and Hare (1976) examined conflict over sex allocation in the social hymenoptera (ants, bees, and wasps). This paper made two key contributions. First, it combined Fisher's (1930) theory of equal investment with Hamilton's (1964) inclusive fitness theory to show how the ES sex allocation differed from the point of view of the queens and their workers. Research on sex allocation conflict within the social hymenoptera has since become the third most productive area in the field of sex allocation (chapter 9). Second, they showed how parent-offspring conflict and inclusive fitness (kin selection) theory could generate predictions that could be tested with empirical data. This was at a time when these topics where still contentious, and to this day, sex allocation still provides some of the clearest support for inclusive fitness theory (sections 9.7.1 and 11.3.1).

Charnov's (1982) monograph, The Theory of Sex Allocation, brought all this together, providing a masterly synthesis of theoretical and empirical work. He unified the different areas of sex allocation research into a single field. From a theoretical perspective, Charnov showed how the same underlying concepts and similar mathematical models could be applied to all of the problems of sex allocation. From an empirical perspective, Charnov's monograph showed the power of selection thinking and simple models to make predictions that could be tested with empirical data, and it led to a surge of interest in sex allocation that continues to this day (Frank 2002; Hardy 2002). The increase in interest in this area is demonstrated by the increasing number of citations per year-comparing 2007 with 1982, the number of citations produced by a Web of Knowledge search on the phrase "sex allocation" has increased 50-fold, and the number of citations produced by a search on the phrases "sex allocation" or "sex ratio" has doubled (subject areas: zoology, genetics and heredity, evolutionary biology, behavioral sciences, plant biology). Charnov's monograph also contained a wealth of leads to potentially useful biological systems that remain underexploited to this day.

1.2.2 Post-Charnov

In the 1980s, our theoretical understanding of LMC leaped forward. At a very general level, the reasons for the female biased sex ratio were clarified, disentangling the separate effects of competition between males, the availability of mates for those males, and inbreeding (section 4.2; Taylor 1981a; Frank 1985b; Herre 1985; Frank 1986a). In addition to settling a long-running controversy, this work solved the debate over the level at which selection operates (Frank 1986a), which sadly still persists in other areas (section At a more specific level, a number of workers began extending LMC theory to fit the biology of specific systems (Werren 1980a; Green et al. 1982; Werren 1984a; Frank 1985b; Herre 1985; Yamaguchi 1985). This generated a slew of new predictions, which allowed for some of the most elegant tests of LMC theory in a wide range of organisms, and such work is still extremely active today (chapter 5).

Following Charnov's monograph, there was a profusion of empirical studies testing the various forms of Trivers and Willard's (1973) hypothesis. The most famous of these was the work of Clutton-Brock and colleagues on red deer, which provided support for both the assumptions and the predictions of Trivers and Willard's hypothesis in response to maternal quality (Clutton-Brock et al. 1984, 1986). This work has inspired many researchers over the years, and an extensive literature on sex allocation in ungulates has accumulated (section 6.4; Sheldon and West 2004). Equally impressive were two long-term studies on species with ESD, one by Conover and colleagues on a fish (section 6.7.2; Conover and Kynard 1981; Conover 1984; Conover and Heins 1987a) and one by Adams and colleagues on a shrimp (section 6.7.1; Naylor et al. 1988a; Naylor et al. 1988b; Watt and Adams 1994; McCabe and Dunn 1997; Dunn et al. 2005). These studies showed the pattern of ESD, the fitness consequences, and why the pattern of ESD should vary across populations.

Our understanding of selfish sex ratio distorters was revolutionized in the 1980s and 1990s (chapter 10). Relatively little was known about distorters at the time of Charnov's (1982) monograph; they were assumed to be rare aberrations. Appreciation of their importance started to emerge, however, with Werren and Skinner's discovery that three different sex ratio distorters occurred in the parasitoid wasp Nasonia vitripennis (Werren et al. 1981; Skinner 1982, 1985). This discovery was shocking because Nasonia had been intensively studied as a model species for understanding LMC and had provided some of the best evidence that individuals adjust offspring sex ratios in response to environmental conditions (Werren 1980a, 1983). The next major jump into the sex allocation limelight for sex ratio distorters was the discovery that endosymbiotic bacteria such as Wolbachia and Cardinium were responsible for many cases of sex ratio distortion and that these endosymbionts were extremely widespread (chapter 9; Rousset et al. 1992; Stouthamer et al. 1993; Werren et al. 1995; Weeks et al. 2003). There is now an extensive literature on sex ratio distorters, with recent work by G. Hurst and colleagues demonstrating how we can even follow their spread and suppression in natural populations (section 10.3.3).

The other major development of the 1980s was an understanding of the population-level consequences of individual-level sex ratio adjustment (section 7.2). Frank (see Frank 1987b; Frank and Swingland 1988; Frank 1990) showed that Trivers and Willard-type sex ratio adjustment can lead to a bias in the population sex ratio or the overall population investment ratio. He also showed that the direction and magnitude of this bias could be hard to predict, depending on biological details that could be hard or impossible to assess. A consequence of this, which is still rarely appreciated, is that population-level patterns will often be useless for testing whether sex allocation is being adjusted facultatively in response to local conditions. Frank, Charnov, and Bull also showed that an important exception to this is in sex changing organisms, where we can make and test predictions about the population sex ratio (section 7.2.3; Frank and Swingland 1988; Charnov 1989; Charnov and Bull 1989a, 1989b; Charnov 1993; Allsop and West 2004b).

Research on sex allocation conflict between individuals really took off in the 1990s (section 9.6). Trivers and Hare's (1976) paper had attracted much interest, but there are limitations on the testability of their predictions using population-level data. Boomsma and Grafen (see Boomsma and Grafen 1990; Boomsma 1991; Boomsma and Grafen 1991) solved this by showing that a range of more specific predictions could be made for how sex allocation should vary between colonies, within a population. In particular, they predicted that if workers were in control of sex ratio in a colony, we should observe split sex ratios, with some colonies producing predominantly male reproductives and others predominantly female (section 9.6.2). Stunning support for their predictions rapidly followed from both observational and experimental studies (section 9.6.3; Mueller 1991; Sundstrom 1994; Evans 1995). Since then, an impressive level of understanding has been obtained in this area by looking at the underlying mechanisms, finer levels of within-colony adjustment, mistakes, and situations where the workers do not win (sections 9.6.4-6; Sundstrom et al. 1996; Sundstrom and Boomsma 2000; Passera et al. 2001; Boomsma et al. 2003). A new area of research on conflict was also opened up by the work of Strand and colleagues showing the potential for sex allocation conflict in polyembryonic wasps and how this might lead to the evolution of a sterile worker caste (section 9.5; Grbic et al. 1992; Giron et al. 2004; Gardner et al. 2007a).

The 1990s saw the conventional wisdom on sex ratio adjustment in vertebrates overturned. It had long been assumed that chromosomal (genetic) sex determination (CSD) in vertebrates such as birds and mammals would prevent adaptive control of offspring sex ratios (Williams 1979). This conception was clearly blown out of the water by a number of studies, primarily on birds. Komdeur and colleagues showed that Seychelles warblers were capable of adjusting the proportion of males in a clutch from between 10% and 90%, depending on environmental conditions (section; Komdeur 1996; Komdeur et al. 1997; Komdeur 1998; Komdeur and Pen 2002). Sex allocation is adjusted in the Seychelles warbler in response to cooperation and competition with offspring. Another area of sex ratio adjustment in birds was opened up by Sheldon and colleagues, who showed that females in species such as collared flycathers and blue tits can adjust the sex of their offspring in response to mate quality, with females producing a higher proportion of sons when they mated with more attractive males (section 6.6; Ellegren et al. 1996; Sheldon et al. 1999). This work was built upon previous findings by Burley (1981) that were so revolutionary in their time that they had been effectively ignored for 15 years. The patterns of sex ratio adjustment in response to helping and male attractiveness have since been shown to be repeatable within and across species, proving clear evidence for control of offspring sex ratios in species with CSD (section 6.6; West and Sheldon 2002).


Excerpted from Sex Allocation by STUART A. WEST Copyright © 2009 by Princeton University Press. Excerpted by permission.
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Table of Contents

Acknowledgments xi

Chapter 1: Sex Allocation 1
1.1 What Is Sex Allocation? 1
1.2 A Potted History 2
1.3 Why Is This Book Needed? 8
1.4 What Is in This Book 8
1.5 What Is Not in This Book 10
1.6 How To Read This Book 11
1.7 Language and Sex Ratios 12

Chapter 2: The Düsing-Fisher Theory of Equal Investment 14
2.1 Introduction 14
2.2 Fisher's Theory of Equal Investment 15
2.3 Darwin to Today 16
2.4 Differential Mortality 19
2.5 Testing Fisher's Theory 20
2.6 Conclusions and Future Directions 31

Chapter 3: Interactions between Relatives I: Cooperation and Competition 33
3.1 Introduction 33
3.2 Basic Theory 34
3.3 Local Resource Enhancement 40
3.4 Local Resource Competition 53
3.5 Conclusions and Future Directions 69

Chapter 4: Interactions between Relatives II: Local Mate Competition 73
4.1 Introduction 73
4.2 Classic Local Mate Competition Theory 74
4.3 Empirical Tests of Local Mate Competition Theory across Populations or Species 83
4.4 Facultative Adjustment of Offspring Sex Ratios by Individuals 93
4.5 Conclusions and Future Directions 107

Chapter 5: Interactions between Relatives III: Extended Local Mate Competition Theory 109
5.1 Introduction 109
5.2 Partial LMC 110
5.3 Variable Clutch Size 116
5.4 Sibmating and Split Sex Ratios in Haplodiploids 131
5.5 Inbreeding Depression 134
5.6 Limited Dispersal and Relatedness between Foundress Females 136
5.7 Haystacks 140
5.8 Asymmetrical Larval Competition 143
5.9 Fertility Insurance 143
5.10 Variance and Precision 151
5.11 Other Population Structures 154
5.12 Stochasticity 155
5.13 Conclusions and Future Directions 156

Chapter 6: Conditional Sex Allocation I: Basic Scenarios 162
6.1 Introduction 162
6.2 Theory 165
6.3 Solitary Parasitoid Wasps and Host Size 167
6.4 Maternal Quality in Ungulates 174
6.5 Maternal Quality and Related Factors in Nonungulates 182
6.6 Mate Attractiveness in Birds and Lizards 187
6.7 Environmental Sex Determination 191
6.8 Sex Change 198
6.9 Conclusions and Future Directions 205

Chapter 7: Conditional Sex Allocation II: Population Consequences and Further Complications 210
7.1 Introduction 210
7.2 Population-Level Patterns 211
7.3 Sex Change Complications 225
7.4 ESD Complications, Especially in Reptiles 243
7.5 Multiple Selective Forces: LMC and Host Size in Parasitoid Wasps 251
7.6 Simultaneous Hermaphrodites 254
7.7 Conclusions and Future Directions 255

Chapter 8: Sex Allocation When Generations Overlap 257
8.1 Introduction 257
8.2 Exceptional Mortality 258
8.3 Exceptional Recruitment 263
8.4 Cyclical Models 265
8.5 Conclusions and Future Directions 273

Chapter 9: Conflict I: Between Individuals 276
9.1 Introduction 276
9.2 Conflict under Fisherian Selection 277
9.3 Conflict under LMC, LRC, and LRE 278
9.4 Sibling Conflict in Haplodiploids and Single-Sex Broods 281
9.5 Polyembryonic Parasitoids 282
9.6 Sex Allocation Conflicts in the Eusocial Hymenoptera 287
9.7 Conclusions and Future Directions 311

Chapter 10: Conflict II: Sex Allocation Distorters 316
10.1 Introduction 316
10.2 Classification of Sex Ratio Distorters 317
10.3 Case Studies 329
10.4 Consequences of Sex Ratio Distorters 344
10.5 Conclusions and Future Directions 351

Chapter 11: General Issues 353
11.1 Introduction 353
11.2 The Success of Sex Allocation 354
11.3 The Use of Sex Allocation 355
11.4 Outstanding Problems 375

References 379
Index 463

What People are Saying About This


This is a great book. It captures the excitement of sex-allocation research, the significant progress that has been made, and the areas that have been relatively neglected. West does a great job of showing the tight connection between evolutionary theory and empirical testing, and the ways both can mutually inspire each other. He deals with all the major issues and guides the reader through the entire field.
Jacobus J. Boomsma, University of Copenhagen


West has great command of a vast body of theory and empirical work, but this book does more than synthesize existing literature. West explains what has been accomplished, where the field has failed to clear things up, and what needs to be done. Anyone working on sex allocation can start with this book and get a firm grasp of the concepts, experiments, comparative observations, and key outstanding questions.
Steven A. Frank, University of California, Irvine

From the Publisher

"This is a great book. It captures the excitement of sex-allocation research, the significant progress that has been made, and the areas that have been relatively neglected. West does a great job of showing the tight connection between evolutionary theory and empirical testing, and the ways both can mutually inspire each other. He deals with all the major issues and guides the reader through the entire field."—Jacobus J. Boomsma, University of Copenhagen

"West has great command of a vast body of theory and empirical work, but this book does more than synthesize existing literature. West explains what has been accomplished, where the field has failed to clear things up, and what needs to be done. Anyone working on sex allocation can start with this book and get a firm grasp of the concepts, experiments, comparative observations, and key outstanding questions."—Steven A. Frank, University of California, Irvine

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