Sexual Conflict

by Göran Arnqvist, Locke Rowe

Overview

The past decade has seen a profound change in the scientific understanding of reproduction. The traditional view of reproduction as a joint venture undertaken by two individuals, aimed at replicating their common genome, is being challenged by a growing body of evidence showing that the evolutionary interests of interacting males and females diverge. This book demonstrates that, despite a shared genome, conflicts between interacting males and females are ubiquitous, and that selection in the two sexes is continuously pulling this genome in opposite directions. These conflicts drive the evolution of a great variety of those traits that distinguish the sexes and also contribute to the diversification of lineages. Göran Arnqvist and Locke Rowe present an array of evidence for sexual conflict throughout nature, and they set these conflicts into the well-established theoretical framework of sexual selection.


The recognition of conflict between the sexes is transforming our theories for the evolution of mating systems and the sexes themselves. Written by two top researchers in the field, Sexual Conflict is the first book to describe this transformation. It is a must read for all scholars and students interested in the evolutionary biology of reproduction.

Product Details

ISBN-13:	9780691122182
Publisher:	Princeton University Press
Publication date:	07/25/2005
Series:	Monographs in Behavior and Ecology , #27
Pages:	352
Product dimensions:	6.00(w) x 9.25(h) x (d)

About the Author

Göran Arnqvist is an associate professor in the Department of Animal Ecology at the University of Uppsala. Locke Rowe is Professor and Canada Research Chair in the Department of Zoology at the University of Toronto.

Read an Excerpt

Sexual Conflict

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By Gran Arnqvist Locke Rowe

Princeton University Press

Copyright © 2005 Princeton University Press
All right reserved.
ISBN: 978-0-691-12218-2

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Chapter One

SEXUAL CONFLICT IN NATURE

During the mating season, male robber flies roam through the vegetation in search of females. When approached by a male, a female takes to the wing, and the male pursues. If overtaken and grappled by a male, females of most species struggle violently, often successfully, to free themselves. In a few species, however, females may use another strategy to achieve the same result; if grasped by a male, they play dead! Once a female stops moving, a male apparently no longer recognizes her as a potential partner, loses interest, and releases the female, who falls to the ground and flies off.

Over the course of the egg-laying period, a male penduline tit (a song bird) makes repeated forays to his partner's nest in an apparent attempt to assess how many eggs she has laid thus far. Female partners, however, seem to make sure that this inspection job is not an easy one for males. Females bury their eggs in the bottom of the nest, perhaps to hide them, and become aggressive toward their mates. Observations in aviaries have shown that these inquisitive males are sometimes injured or even killed by their secretive mates.

As in most spiders where courting males are at risk of being cannibalized by females, a male of thefunnel-web spider Agelenopsis aperta approaches a female slowly and very carefully. Once close, he sprays an apparent "toxin" at the female, which makes her (and occasionally him) collapse and enter an "unconscious" state. The male then hauls the cataleptic female about the web, repositions her, and finally inseminates her while she is still "knocked out." At the time of mating, a male Malabar ricefish will dart toward a nearby female with near-lightning speed. Dashing toward the female from below, he strikes her in the genital region with a complex clublike organ. If the organ, a modified anal fin, contacts the female body, it releases a spermatophore (a sperm capsule) with a dartlike spike. This spike is pushed into the female flesh, and the spermatophore becomes firmly attached because of a whorl of recurved barbs at its tip. Females are adapted to these repeated assaults; they can be found with multiple attached spermatophores, and the skin around their genital pore is markedly thickened and hardened.

If one looks closely enough, observations such as these abound in the biological literature. But what do we make of these? It is difficult to reconcile observations of open conflict between the sexes with the common view of mating as a joint venture of two individuals that, by virtue of being the same species, share a common genome. Often, those cases where male-female interactions involve overt coercion, manipulation, deceit, or harm have been stowed away and otherwise obscured. If explanations are offered, they often rest on special circumstances.

The main message of this book is that, despite interacting males and females sharing the same genome, conflict between them is ubiquitous. In other words, some genes expressed in females will be in conflict with others expressed in males. Moreover, some genes expressed in both sexes may be favored to do divergent things when expressed in females and in males. Selection on these genes is therefore sexually antagonistic. We will argue that the robber flies, penduline tits, funnel-web spiders, and ricefish may all have something very important to tell us. That is, how males and females came to be the way they are.

1.1 Evolving Views of Sex and Reproduction

Biologists and laypeople have long regarded mating as a largely harmonious event in which males and females cooperate in producing offspring. In fact, if we assume the entire result of mating is the production of shared offspring, it is not immediately obvious why we should think otherwise. Embedded in this view may be an assumption of monogamy, where the reproductive success of each individual of the pair is equal to, and contingent upon, the other individual. In these cases, if one can elevate the reproductive success of a partner, both will reap equal benefits. If we accept all of this, it is easy to imagine that what is good for one partner is good for the other and, in fact, also good for the species. These three perceptions-harmony in sexual interactions, monogamy, and a concordance between what is good for the individual and the species-have a long history but are often incorrect.

Evolutionary views of the interactions between the sexes have been fundamentally influenced by the work of Charles Darwin. Darwin often portrays reproduction in general and sex in particular as being something essentially reserved for the monogamous and married couple. In his famous 1871 book The Descent of Man and Selection in Relation to Sex, he summarizes an experiment involving a small crustacean as follows: "The female, when thus divorced, soon joined the others. After a time the male was put again into the same vessel; and he then, after swimming about for a time, dashed into the crowd, and without any fighting at once took away his wife." Darwin did recognize the existence of polygamy, as evidenced in a letter to his friend Charles Lyell, where he describes female barnacles as having "two little pockets, in each of which she kept a little husband." Yet, he was clearly reluctant to entertain the idea that the "practice of polygamy" was widespread, and even saw this as the major problem for his theory of sexual selection. "Our difficulty in regard to sexual selection lies in understanding how it is that the males which conquer other males, or those which prove the most attractive to the females, leave a greater number of offspring to inherit their superiority than their beaten and less attractive rivals. Unless this result does follow, the characters which give to certain males an advantage over others, could not be perfected and augmented through sexual selection. When the sexes exist in exactly equal numbers, the worst-endowed males will (except where polygamy prevails), ultimately find females, and leave as many offspring, as well fitted for their general habits of life, as the best-endowed males." Today, thanks in part to the advent of DNA fingerprinting, we know that true genetic monogamy is in fact extremely rare (Birkhead 1997). In the absence of monogamy, as we will see, partnerships are temporary and the lifetime reproductive success of partners is no longer equal.

It is equally clear from Darwin's writings and in line with the general moral that he considered interactions between the sexes to be inherently good; an "aid to ordinary [natural] selection." By this we mean that events leading to mating, such as female choice of certain males or competition among males for access to females, work hand in hand with natural selection to improve the adaptedness of the lineage: "Just as man can improve the breeds of his game-cocks by the selection of those birds which are victorious in the cockpit, so it appears that the strongest and most vigorous males, or those provided with the best weapons, have prevailed under nature, and have led to the improvement of the natural breed or species." Darwin's own theories were likely influenced by the writings of his grandfather Erasmus Darwin. In his book Zoonomia (1794), he argued that the "purpose" of reproductive competition is to improve the species. "The final cause of this contest amongst the males seems to be that the strongest and most active animal should propagate the species, which should thence become improved." This heritage is echoed in two prevalent ideas in modern evolutionary biology, which both ascribe similar utility to reproductive interactions. One concerns the hypothesis that male secondary sexual traits used in reproductive competition are "honest indicators" of male genetic quality, which enable females to select the males with the "best" genes as fathers for their offspring (Zahavi 1975). The other poses that male sexual traits function to "preserve the species," i.e., by allowing species recognition and hybridization avoidance (Mayr 1940, Lack 1968), and the linked belief among ethologists in the 1950s and 1960s that male courtship functions to allow the female to choose a male of the correct species and strengthen conspecific pair bonds.

Theoretical analyses of the consequences of male-female coevolutionary interactions confirm, in some cases, Darwin's assertion that sexual selection works in lockstep with natural selection to increase population fitness (e.g., Siller 2001, Agrawal 2001, Lorch et al. 2003). But, in other cases, the opposite is true; the outcome of coevolution between the sexes is to decrease the fitness of populations (Lande 1981, Gavrilets et al. 2001, Kokko and Brooks 2003). Yet this latter result has not been widely acknowledged. Perhaps it is simply that evolutionary change is just thought of as an inherently good thing! This underlying belief has sometimes been obvious to us when describing our own work on water striders to the public and some colleagues. In these species males grasp females without prior courtship and females struggle vigorously to get rid of males. Male mating attempts can be accounted for by selection to fertilize more eggs, and female resistance of these repeated male mating attempts can be accounted for because they are both superfluous and costly (e.g., Rowe et al. 1994, Arnqvist 1997a). Our studies suggest that both sexes have accumulated antagonistic adaptations, in a form of coevolutionary "arms race," that further their interests but at the same time are costly. The idea that mating interactions might cause the evolution of decreased fitness in a population has been particularly difficult for people to entertain, public and scholars alike, and has sometimes even been considered antiadaptationist.

The understanding among many biologists of male-female interactions has, nevertheless, changed over the last two decades. The view of reproduction as an exclusively cooperative endeavor has been challenged by the realization that the mates' interests in any interaction are often conflicting. Tracing the history of this shift is not easy. Although a few early contributions hinted at sexual conflict (e.g., Wickler 1968), the major players certainly include Robert Trivers, Richard Dawkins, and Geoff Parker. Robert Trivers (1972) was the first to provide a compelling evolutionary discussion of differences between the evolutionary interests of the sexes and the implications this might have for the evolution of parental care in particular. Richard Dawkins put the idea of sexual conflict before a wide audience-most notably in a book chapter entitled "Battle of the Sexes" in his widely read 1976 book The Selfish Gene, but also in a few other early contributions (e.g., Dawkins and Krebs 1978, 1979).

There is, however, no doubt that the most thorough discussion of the role of sexual conflict in the evolution of the sexes was a contribution by Geoff Parker, which was unfortunately published in a little-known book (Parker 1979). Although Parker (1979) made "no claim to originality for the suggestion that this asymmetry [in the relative interests of the sexes] can occur commonly in animals," certainly he contributed more than anyone else to the introduction and subsequent development of the field. This material was first drafted several years prior to its publication, and Parker's ideas likely influenced many other early thinkers in the field. Most ideas expressed by Parker (1979) were much ahead of their time. His landmark paper remains arguably underutilized, although it has recently begun to draw the attention it deserves (figure 1.1). Parker has continued to build the field with a steady flow of influential contributions regarding conflict in his model system, dungflies, and more generally with new theory (see the list of references). During the 1980s, the concept of sexual conflict was given some attention in the theoretical literature, but empirical work on conflict and its consequences remained very rare. It was not until the 1990s that research on sexual conflict hit the mainstream of research in ecology and evolution, and interest has since increased dramatically. Why this sudden increase in attention?

We believe that several more or less coinciding factors have contributed to the almost explosive growth of the field. Students of animal behavior began focusing on females as active participants in coevolutionary interactions with males (e.g., Hrdy 1981, Kirkpatrick 1987a,b, Ahnesjö et al. 1993, Eberhard 1996, Gowaty 1997a, 2003, Zuk 2002). This fact may have resulted in part from philosophical shifts in thinking brought about by the feminist movement. The focus on the selective forces acting upon females in their interactions with males revealed that selection was often sexually antagonistic. Comprehensive data illustrating this point in dungflies were collected by Parker in the late 1960s (Parker 1970a,b) and began accumulating for a few other model organisms (e.g., Alatalo et al. 1981, Rowe et al. 1994, Clutton-Brock and Parker 1995). The work by Linda Partridge and coworkers on fruit flies, demonstrating male-imposed costs of mating for females, was particularly influential (e.g., Partridge et al. 1986, 1987, Fowler and Partridge 1989, Chapman et al. 1995). Despite the accumulating evidence, studies remained relatively rare, and most centered on insect behavior. One notable exception was a laboratory experimental evolution study of sexual conflict in flies (Rice 1996b).

This situation changed noticeably with the publication of a perspective by Brett Holland and Bill Rice in 1998. In this paper, they persuasively laid out the case for sexually antagonistic coevolution and did so with examples from favored taxa for studies of sexual interactions, such as birds and fishes. This paper certainly brought the evolutionary potential of sexual conflict to a much wider audience. Since then, the scope of study has increased not just taxonomically, but also in level of analysis. Molecular studies showing positive selection on, and rapid evolution of, reproductive proteins are now being interpreted as evidence of sexual conflict (see Chapman 2001, Swanson and Vacquier 2002). New theory suggests that sexual conflict has profound implications for the evolution of reproductive isolation and speciation itself (Rice 1998a, Parker and Partridge 1998). These facts reinforce the view that sexual conflict may be playing a central role in evolution within and between species. Today, the field is still rapidly expanding and filled with lively debate (Zeh and Zeh 2003). Hopefully, these accumulating data and debates will enrich our understanding of the biology of male-female interactions, and the evolution of the sexes themselves.

1.2 Sexually Antagonistic Selection and Sexual Conflict

The evolutionary interests of any two individuals are rarely, if ever, identical. This must be true, simply because they do not share the same alleles for all loci, with the possible exception of clones. Where alleles at a locus differ, there will be competition among them. Therefore, the evolutionary interests of any two individuals have the potential to conflict, even if they share much of the same genome. When two unrelated individuals of the two sexes meet to engage in sexual reproduction, conflict intensifies: while one individual needs the other to spread its genes, this dependence may be asymmetric. Further, although both have a shared interest in any mutual offspring, they usually have divergent interests in many aspects of the "economics" of reproduction. Defined as a conflict between the evolutionary interests of individuals of the two sexes (Parker 1979), sexual conflict becomes exacerbated because selection will often be tugging in different directions in the two sexes. Sexually antagonistic selection is symptomatic of sexual conflict. We expect sexually antagonistic selection to be common simply because the "roles" of the sexes in reproduction differ (Clutton-Brock 1991, Andersson 1994), and sexual conflict should be a general feature in the evolution of the two sexes.

Conflict between coreproducing individuals occurs also in isogamous species (gametes of equal size), because increased investment by one partner permits decreased investment by the other. In fact, there are good reasons to believe that "primordial" reproductive conflict in isogamous taxa has led to the evolution of anisogamy, and consequently the sexes (see Parker et al. 1972, Parker 1979, 1984, Bulmer and Parker 2002). Because males and females, by definition, produce gametes of different size (anisogamy), they typically maximize their reproductive success in more or less different ways. A classic example of this is the fact that, over much of the natural range of mating frequencies, the number of offspring produced generally increases monotonically with the number of mates in males but not in females (Bateman 1948). When this is so, there is selection favoring increased mating frequency in males, but not females. The fact that the sexes thus "play" very different roles during reproduction then sets the scene for differences in physiology, morphology, and behavior between males and females. This fact also means that the attributes or trait values favored in one sex are often not those favored in the other. Consequently, there will be sexually antagonistic selection on these traits. As such, some degree of sexual conflict will be ubiquitous in sexually reproducing taxa (Trivers 1972, Parker 1979, Lessels 1999).

(Continues...)

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Table of Contents

Preface xi
Chapter 1: Sexual Conflict in Nature 1
1.1 Evolving Views of Sex and Reproduction 2
1.2 Sexually Antagonistic Selection and Sexual Conflict 6
1.2.1 Intralocus Sexual Conflict 7
1.2.2 Interlocus Sexual Conflict 10
1.3 Aims and Scope 11
Chapter 2: Sexual Selection and Sexual Conflict: History,Theory,and Empirical Avenues 14
2.1 Darwin ’s Views on Sexual Selection 14
2.2 The Fisher Process 18
2.3 Indicator,or Good Genes,Mechanisms 22
2.4 The Male Trait 25
2.5 Direct Benefits 26
2.6 Preexisting Biases and the Origin of the Preference 27
2.7 Sexual Conflict 29
2.7.1 Parker’s Initial Models of Sexual Conflict 30
2.7.2 Genetic Models 31
2.7.3 Phenotype-Dependent and Phenotype-Independent Costs 34
2.7.4 Nonequilibrium Models 35
2.8 Sexual Conflict Set in the Framework of Sexual Selection 35
2.9 The Roles of the Sexes in Sexual Conflict 38
2.10 Empirical Approaches to the Study of Sexual Conflict 40
Chapter 3: Sexual Conflict Prior to Mating 44
3.1 The Economy of Mating and the Evolution of Resistance 45
3.1.1 Direct Costs of Mating 45
3.1.2 Costs of Low Mate Quality 46
3.1.3 Costs of Resisting Mating 47
3.1.4 Costs to Females as a Side Effect of Male-Male Competition 48
3.1.5 Sexual Conflict and the Evolution of Sexual Cannibalism by Females 50
3.1.6 Sexual Conflict and the Evolution of Infanticide by Males 53
3.2 Adaptations for Persistence and Resistance 55
3.2.1 Harassment and Resistance 57
3.2.2 Grasping Traits 60
3.2.3 Antigrasping Traits and Other Forms of Resistance 68
3.2.4 Exploitation of Sensory Biases 71
3.2.5 Convenience Polyandry 77
3.3 Sexual Conflict and Sexual Selection 78
3.4 Mate “Screening” and Other Alternative Explanations for Resistance Traits 80
3.5 Case Studies in Sexually Antagonistic Coevolution 83
3.5.1 Diving Beetles 83
3.5.2 Water Striders 84
3.5.3 Bedbugs 87
Chapter 4: Sexual Conflict after Mating 92
4.1 Female Reproductive Effort and the Conflicting Interests of the Sexes 96
4.1.1 Seminal Substances with Gonadotropic Effects 97
4.1.2 Nuptial Feeding 102
4.1.3 Male Display Traits 103
4.2 Female Mating Behavior, Sperm Competition, and the Conflicting Interests of the Sexes 106
4.2.1 Male Defensive Adaptations and Sexual Conflict 107
4.2.1.1 Costs of Delaying Remating in Females 111
4.2.1.2 Female Costs as Side Effects 116
4.2.1.3 Female Costs as a Direct Target of Male Strategies 118
4.2.2 Male Offensive Adaptations and Sexual Conflict 121
4.2.2.1 Sperm Competition and Aggressive Ejaculates 121
4.2.2.2 Direct Costs, Polyspermy, and Female Infertility 122
4.2.2.3 Indirect Costs and Deleterious Matings 128
4.2.2.4 Conflicts over Cryptic Female Choice 129
4.3 Conflicts over the Duration of Mating 132
4.3.1 Male and Female Adaptations 135
4.4 Postmating Conflicts and Male-Female Coevolution 139
4.5 Elaborated Male Ejaculates: Nuptial Gifts or Medea Gifts? 140
4.6 Are Male Postmating Adaptations Costly to Females? 146
4.7 It Takes Two to Tango: Sexually Antagonistic Coevolution in Fruit Flies 149
Chapter 5: Parental Care and Sexual Conflict 156
5.1 The Basic Conflict 156
5.2 Mate Desertion 158
5.2.1 Conflict over Care and Desertion in Uniparental Species 158
5.2.2 Never Trust a Penduline Tit! 160
5.3 “Partial ”Mate Desertion and Sexual Conflict over the Mating System in Biparental Species 164
5.4 Sexual Conflict over the Relative Amount of Care in Biparental Monogamous Species 170
5.5 The Dunnock: Family Life in Cambridge University Botanic Garden 174
Chapter 6: Other Implications of Sexual Conflict 179
6.1 The Evolution of Genomic Imprinting 179
6.2 Sexual Conflict, Sex Ratios, and Sex Allocation 183
6.3 Dueling Worms and Stabbing Snails: Sexual Conflict within Hermaphrodites 185
6.3.1 Premating Conflict in Hermaphrodites 187
6.3.2 Postmating Conflict in Hermaphrodites 190
6.3.3 Sexual Selection and Antagonistic Coevolution in Hermaphrodites 192
6.3.4 The Love Dart in Snails—A Shot at Paternity? 196
6.4 Sexual Conflict in Plants 200
6.5 Sexual Conflict, Speciation, and Extinction 203
6.5.1 Sexual Conflict as an Engine of Evolutionary Divergence 207
6.5.2 Population Crosses—Inferring Process from Pattern 210
6.6 Sexual Conflict and Sex Chromosomes 212
Chapter 7: Concepts and Levels of Sexual Conflict 216
7.1 Levels of Analysis 216
7.2 Resolution of Sexual Conflict 219
7.3 Winners and Losers of Sexual Conflict? 220
7.4 Sexual Conflict over the Control of Interactions 222
7.5 The Intensity of Sexual Conflict 223
7.6 Sexual Conflict over Mate Choice 224
Chapter 8: Concluding Remarks 226
References 229
Author Index 305
Subject Index 321

What People are Saying About This

William Rice

This book represents an important contribution in synthesizing a new field of study. The authors have for example done an outstanding job of integrating hundreds of studies, published in a broad diversity of unrelated journals, into the context of intersexual conflict. Their presentation of pertinent empirical studies provides an unprecedented wealth of valuable information.
— William Rice, University of California, Santa Barbara

Tom Tregenza

This book addresses a very topical field within evolutionary biology—the existence of conflicts of interest between mates. Indeed it provides the first substantial review of the natural history and evolutionary dynamics of sexual conflict. Cogently and articulately argued, it will no doubt become essential reading for all those interested in the subject.
— Tom Tregenza, University of Exeter in Cornwall

From the Publisher

"This book addresses a very topical field within evolutionary biology—the existence of conflicts of interest between mates. Indeed it provides the first substantial review of the natural history and evolutionary dynamics of sexual conflict. Cogently and articulately argued, it will no doubt become essential reading for all those interested in the subject."—Tom Tregenza, University of Exeter in Cornwall

"This book represents an important contribution in synthesizing a new field of study. The authors have for example done an outstanding job of integrating hundreds of studies, published in a broad diversity of unrelated journals, into the context of intersexual conflict. Their presentation of pertinent empirical studies provides an unprecedented wealth of valuable information."—William Rice, University of California, Santa Barbara

Editorial Reviews

"Sexual Conflict offers an alternative interpretation of the idea of co-operation between males and females. . . . [It] provides a convincing account of an antagonistic relationship driving evolution. It sets out to illustrate the ubiquitous nature of sexual conflict and persuasively presents the evidence for this, concluding that traditional views of peaceful co-operation are perhaps not as accurate as once believed."—-Helen L. Kroening, Biologist

From the Publisher

Sexual Conflict offers an alternative interpretation of the idea of co-operation between males and females. . . . [It] provides a convincing account of an antagonistic relationship driving evolution. It sets out to illustrate the ubiquitous nature of sexual conflict and persuasively presents the evidence for this, concluding that traditional views of peaceful co-operation are perhaps not as accurate as once believed.
— Helen L. Kroening

Biologist

Sexual Conflict offers an alternative interpretation of the idea of co-operation between males and females. . . . [It] provides a convincing account of an antagonistic relationship driving evolution. It sets out to illustrate the ubiquitous nature of sexual conflict and persuasively presents the evidence for this, concluding that traditional views of peaceful co-operation are perhaps not as accurate as once believed.

Biologist - Helen L. Kroening