How does breeding system variation modulate sexual antagonism?

The study of sexually antagonistic (SA) traits remains largely limited to dioecious (separate sex), mobile animals. However, the occurrence of sexual conflict is restricted neither by breeding system (the mode of sexual reproduction, e.g. dioecy or hermaphroditism) nor by sessility. Here, we synthesize how variation in breeding system can affect the evolution and expression of intra- and inter-locus sexual conflicts in plants and animals. We predict that, in hermaphrodites, SA traits will (i) display lower levels of polymorphism; (ii) respond more quickly to selection; and (iii) involve unique forms of interlocus conflict over sex allocation, mating roles and selfing rates. Explicit modelling and empirical tests in a broader range of breeding systems are necessary to obtain a general understanding of the evolution of SA traits.     

Perspective: sexual conflict and sexual selection: chasing away paradigm shifts

Abstract.— Traditional models of sexual selection propose that partner choice increases both average male and average female fitness in a population. Recent theoretical and empirical work, however, has stressed that sexual conflict may be a potent broker of sexual selection. When the fitness interests of males and females diverge, a reproductive strategy that increases the fitness of one sex may decrease the fitness of the other sex. The chase-away hypothesis proposes that sexual conflict promotes sexually antagonistic, rather than mutualistic, coevolution, whereby manipulative reproductive strategies in one sex are counteracted by the evolution of resistance to such strategies in the other sex. In this paper, we consider the criteria necessary to demonstrate the chase-away hypothesis. Specifically, we review sexual conflict with particular emphasis on the chase-away hypothesis; discuss the problems associated with testing the predictions of the chase-away hypothesis and the extent to which these predictions and the predictions of traditional models of sexual selection are mutually exclusive; discuss misconceptions and mismeasures of sexual conflict; and suggest an alternative approach to demonstrate sexual conflict, measure the intensity of sexually antagonistic selection in a population, and elucidate the coevolutionary trajectories of the sexes.     

The ecology of sexual conflict: ecologically dependent parallel evolution of male harm and female resistance in Drosophila melanogaster

The prevalence of sexual conflict in nature, along with the potentially stochastic nature of the resulting coevolutionary trajectories, makes it an important driver of phenotypic divergence and speciation that can operate even in the absence of environmental differences. The majority of empirical work investigating sexual conflict's role in population divergence/speciation has therefore been done in uniform environments and any role of ecology has largely been ignored. However, theory suggests that natural selection can constrain phenotypes influenced by sexual conflict. We use replicate populations of Drosophila melanogaster adapted to alternative environments to test how ecology influences the evolution of male effects on female longevity. The extent to which males reduce female longevity, as well as female resistance to such harm, both evolved in association with adaptation to the different environments. Our results demonstrate that ecology plays a central role in shaping patterns of population divergence in traits under sexual conflict.     

Sexual conflict in a changing environment

Sexual conflict has extremely important consequences for various evolutionary processes including its effect on local adaptation and extinction probability during environmental change. The awareness that the intensity and dynamics of sexual conflict is highly dependent on the ecological setting of a population has grown in recent years, but much work is yet to be done. Here, we review progress in our understanding of the ecology of sexual conflict and how the environmental sensitivity of such conflict feeds back into population adaptivity and demography, which, in turn, determine a population's chances of surviving a sudden environmental change. We link two possible forms of sexual conflict – intralocus and interlocus sexual conflict – in an environmental context and identify major gaps in our knowledge. These include sexual conflict responses to fluctuating and oscillating environmental changes and its influence on the interplay between interlocus and intralocus sexual conflict, among others. We also highlight the need to move our investigations into more natural settings and to investigate sexual conflict dynamics in wild populations.     

Are flies kind to kin? The role of intra- and inter-sexual relatedness in mediating reproductive conflict

As individual success often comes at the expense of others, interactions between the members of a species are frequently antagonistic, especially in the context of reproduction. In theory, this conflict may be reduced in magnitude when kin interact, as cooperative behaviour between relatives can result in increased inclusive fitness. Recent tests of the potential role of cooperative behaviour between brothers in Drosophila melanogaster have proved to be both exciting and controversial. We set out to replicate these experiments, which have profound implications for the study of kin selection and sexual conflict, and to expand upon them by also examining the potential role of kinship between males and females in reproductive interactions. While we did observe reduced fighting and courtship effort between competing brothers, contrary to previous studies we did not detect any fitness benefit to females as a result of the modification of male antagonistic behaviours. Furthermore, we did not observe any differential treatment of females by their brothers, as would be expected if the intensity of sexual conflict was mediated by kin selection. In the light of these results, we propose an alternative explanation for observed differences in male–male conflict and provide preliminary empirical support for this hypothesis.     

Sex‐biased dispersal,kin selection and the evolution of sexual conflict

There is growing interest in resolving the curious disconnect between the fields of kin selection and sexual selection. Rankin's (2011, J. Evol. Biol. 24 , 71–81) theoretical study of the impact of kin selection on the evolution of sexual conflict in viscous populations has been particularly valuable in stimulating empirical research in this area. An important goal of that study was to understand the impact of sex‐specific rates of dispersal upon the coevolution of male‐harm and female‐resistance behaviours. But the fitness functions derived in Rankin's study do not flow from his model's assumptions and, in particular, are not consistent with sex‐biased dispersal. Here, we develop new fitness functions that do logically flow from the model's assumptions, to determine the impact of sex‐specific patterns of dispersal on the evolution of sexual conflict. Although Rankin's study suggested that increasing male dispersal always promotes the evolution of male harm and that increasing female dispersal always inhibits the evolution of male harm, we find that the opposite can also be true, depending upon parameter values.     

Sexually antagonistic evolution caused by male–male competition in the pistil

Although sexual selection and sexual conflict are important evolutionary forces in animals, their significance in plants is uncertain. In hermaphroditic organisms, such as many plants, sexual conflict may occur both between mating partners (interlocus conflict) and between male and female sex roles within an individual (intralocus conflict). We performed experimental evolution, involving lines that were crossed with either one or two pollen donors (monogamous or polyandrous lines), in the hermaphroditic plant (Collinsia heterophylla) where early fertilizations are associated with female fitness costs (reduced seed set). Artificial polyandry for four generations resulted in enhanced pollen performance and increased female fitness costs compared to the monogamous and source (starting material) lines. Female fitness was also reduced in the monogamous line, indicating a possible trade‐off between sex roles, resulting from early pollination. We performed a second experiment to investigate a potential harming effect of pollen performance on seed set. We found that high siring success of early arriving pollen competing with later‐arriving pollen was associated with high female fitness costs, consistent with an interlocus sexual conflict. Our study provides evidence for the importance of sexual selection in shaping evolution of plant reproductive strategies, but also pinpoints the complexity of sexual conflict in hermaphroditic species.     

Intraspecific sperm competition genes enforce post-mating species barriers in Drosophila

Sexual selection and sexual conflict are considered important drivers of speciation, based on both theoretical models and empirical correlations between sexually selected traits and diversification. However, whether reproductive isolation between species evolves directly as a consequence of intrapopulation sexual dynamics remains empirically unresolved, in part because knowledge of the genetic mechanisms (if any) connecting these processes is limited. Here, we provide evidence of a direct mechanistic link between intraspecies sexual selection and reproductive isolation. We examined genes with known roles in intraspecific sperm competition (ISC) in D. melanogaster and assayed their impact on conspecific sperm precedence (CSP). We found that two such genes (Acp36DE and CG9997) contribute to both offensive sperm competition and CSP; null/knockdown lines both had lower competitive ability against D. melanogaster conspecifics and were no longer able to displace heterospecific D. simulans sperm in competitive matings. In comparison, Sex Peptide (Acp70A)—another locus essential for ISC—does not contribute to CSP. These data indicate that two loci important for sperm competitive interactions have an additional role in similar interactions that enforce post-mating reproductive isolation between species, and show that sexual selection and sexual isolation can act on the same molecular targets in a gene-specific manner.     

Sexual conflict and reproductive isolation in flies

Sexual conflict is predicted to generate more rapid reproductive isolation between larger populations. While there is some empirical support for this, the data are inconsistent and, additionally, there has been criticism of some of the evidence. Here we reanalyse two experimental-evolution datasets using an isolation index widely applied in the speciation literature. We find evidence for reproductive isolation through sexual conflict in Sepsis cynipsea, but not in Drosophila melanogaster, and this occurred to a greater degree in larger populations, which is consistent with previous findings.     

Female choice of sexually antagonistic male adaptations: a critical review of some current research

We contrast some recent uses of the concept of male-female conflict, with the type of conflict that is inherent in traditional Darwinian female choice. Females in apparent conflict situations with males may suffer reduced lifetime reproduction, but nevertheless benefit because they obtain sons with superior manipulative abilities. Female defences against male manipulations may not be 'imperfect' because of inability to keep pace with male evolution, but in order to screen males and favour those that are especially good manipulators. We examine the consequences of these ideas, and of the difficulties of obtaining biologically realistic measures of female costs, for some recent theoretical and empirical presentations of male-female conflict ideas, and find that male-female conflict in the new sense is less certain than has been commonly supposed. Disentangling previous sexual selection ideas and the new conflict of interest models will probably often be difficult, because the two types of payoffs are not mutually exclusive.     

Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

Intra-locus sexual conflict results when sex-specific selection pressures for a given trait act against the intra-sexual genetic correlation for that trait. It has been found in a wide variety of taxa in both laboratory and natural populations, but the importance of intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic organisms has rarely been considered. This is not so surprising given the conceptual and theoretical association of intra-locus sexual conflict with sexual dimorphism, but there is no a priori reason why intra-locus sexual conflict cannot occur in hermaphroditic organisms as well. Here, I discuss the potential for intra-locus sexual conflict in hermaphroditic animals and review the available evidence for such conflict, and for the existence of sexually antagonistic genetic variation in hermaphrodites. I argue that mutations with asymmetric effects are particularly likely to be important in mediating sexual antagonism in hermaphroditic organisms. Moreover, sexually antagonistic genetic variation is likely to play an important role in inter-individual variation in sex allocation and in transitions to and from gonochorism (separate sexes) in simultaneous hermaphrodites. I also describe how sequential hermaphrodites may experience a unique form of intra-locus sexual conflict via antagonistic pleiotropy. Finally, I conclude with some suggestions for further research.     

An assessment of Putative Sexually Antagonistic Traits in a Freshwater Amphipod Species

Sexual conflict can result in an ‘evolutionary arms race’ between males and females, with the evolution of sexual antagonistic traits used to resolve the conflict in favor of one sex over the other. We assessed the resolution of sexual conflict in a Hyalella amphipod species by manipulating putative sexually antagonistic traits in males and females and used mate‐guarding duration as our metric of conflict resolution. We discovered that large male posterior gnathopod size increased mate‐guarding duration, which suggests that it is a sexually antagonistic trait in this species. In contrast, female and male body size did not significantly affect mate‐guarding duration. Given that male posterior gnathopods show heightened condition dependence, future investigations should explore the interactive effects of sexual conflict and ecological context on trait evolution, phenotypic divergence, and speciation to elucidate the complex mechanisms involved in the evolution of biological diversity.     

Interactions between genotype and sexual conflict environment influence transgenerational fitness in Drosophila melanogaster

Theory predicts that sexual conflict can fuel evolutionary change and generate substantial reproductive costs. This was tested here by measuring the fitness of focal individuals across multiple generations using an experimental framework. We manipulated sexual conflict through high versus low exposure of females to males across a four-generation pedigree of Drosophila melanogaster, and assessed fitness in 1062 females and 639 males. We used the animal model to estimate (1) genotype by sexual conflict environment interactions for female fitness and (2) indirect benefits gained through sons and daughters. Some female genotypes achieved higher fitness under low, in comparison to high, conflict and vice versa. We found a consistent 10% reduction in female fitness under high conflict, regardless of maternal history. Following high exposure, females produced sons with increased, but grandsons with decreased, fitness. This opposing effect suggests no consistent fitness gains through sons for females that mated multiply. We saw no indirect benefits through daughters. Our pedigree was based exclusively on maternal links; however, maternal effects are unlikely to contribute significantly unless expressed across multiple generations. In sum, we quantified a significant sexual conflict load and a female genotype by sexual conflict interaction that could slow the erosion of genetic variation.     

Sex roles and sex ratios in animals

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.     

Two sexes,one genome: the evolutionary dynamics of intralocus sexual conflict

As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug‐of‐war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex‐specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex‐specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole‐genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra‐ and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex‐specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a “conflict over shared genes.”     

Evidence for strong intralocus sexual conflict in the Indian meal moth, Plodia interpunctella

Males and females share a genome and express many shared phenotypic traits, which are often selected in opposite directions. This generates intralocus sexual conflict that may constrain trait evolution by preventing the sexes from reaching their optimal phenotype. Furthermore, if present across multiple loci, intralocus sexual conflict can result in a gender load that may diminish the benefits of sexual selection and help maintain genetic variation for fitness. Despite the importance of intralocus sexual conflict, surprisingly few empirical studies conclusively demonstrate its operation. We show that the pattern of multivariate selection acting on three sexually dimorphic life-history traits (development time, body size, and longevity) in the Indian meal moth, Plodia interpunctella, is opposing for the sexes. Moreover, we combined our estimates of selection with the additive genetic variance-covariance matrix (G) to predict the evolutionary response of the life-history traits in the sexes and showed that the angle between the vector of responses and the vector of sexually antagonistic selection was almost orthogonal at 84.70°. Thus, G biases the predicted response of life-history traits in the sexes away from the direction of sexually antagonistic selection, confirming the presence of strong intralocus sexual conflict in this species. Despite this, sexual dimorphism has evolved in all of the life-history traits examined suggesting that mechanism(s) have evolved to resolve this conflict and allow the sexes to reach their life-history optima. We argue that intralocus sexual conflict is likely to play an important role in the evolution of divergent life-history strategies between the sexes in this species.     

Indirect genetic effects and sexual conflicts: Partner genotype influences multiple morphological and behavioral reproductive traits in a flatworm

The expression of an individual's phenotypic traits can be influenced by genes expressed in its social partners. Theoretical models predict that such indirect genetic effects (IGEs) on reproductive traits should play an important role in determining the evolutionary outcome of sexual conflict. However, empirical tests of (i) whether reproductive IGEs exist, (ii) how they vary among genotypes, and (iii) whether they are uniform for different types of reproductive traits are largely lacking. We addressed this in a series of experiments in the simultaneously hermaphroditic flatworm Macrostomum lignano. We found strong evidence for IGEs on both morphological and behavioral reproductive traits. Partner genotype had a significant impact on the testis size of focal individuals—varying up to 2.4‐fold—suggesting that IGEs could mediate sexual conflicts that target the male sex function. We also found that time to first copulation was affected by a genotype × genotype interaction between mating partners, and that partner genotype affected the propensity to copulate and perform the postcopulatory suck behavior, which may mediate conflicts over the fate of received ejaculate components. These findings provide clear empirical evidence for IGEs on multiple behavioral and morphological reproductive traits, which suggests that the evolutionary dynamics of these traits could be altered by genes contained in the social environment.     

Sexual conflict in primates

Sexual conflict is increasingly recognized as a major force for evolutionary change and holds great potential for delineating variation in primate behavior and morphology. The goals of this review are to highlight the rapidly rising field of sexual conflict and the ongoing shift in our understanding of interactions between the sexes. We discuss the evidence for sexual conflict within the Order Primates, and assess how studies of primates have illuminated and can continue to increase our understanding of sexual conflict and sexual selection. Finally, we introduce a framework for understanding the behavioral, anatomical, and genetic expression of sexual conflict across primate mating systems and suggest directions for future research.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.