Signature of sexual conflict is actually conflict resolved

There has been substantial interest of late in using population genetic methods to study sexual conflict, where an allele increases the fitness of one sex at some cost to the other (Mank, 2017). Population genomic scans for sexual conflict offer an important advance given the difficulties of identifying antagonistic alleles from more traditional methods, and could greatly increase our understanding of the extent and loci of sexual conflict. This is particularly true for studies in natural populations, for which obtaining accurate fitness measurements for each sex can be challenging. In this issue of Molecular Ecology, Bissegger, Laurentino, Roesti, and Berner (2019) present a cautionary tale about how to interpret these population genomic data.     

Replicator-dynamics models of sexual conflict

Evolutionary conflict between the sexes has been studied in various taxa and in various contexts. When the sexes are in conflict over mating rates, natural selection favors both males that induce higher mating rates and females that are more successful at resisting mating attempts. Such sexual conflict may result in an escalating coevolutionary arms race between males and females. In this article, we develop simple replicator-dynamics models of sexual conflict in order to investigate its evolutionary dynamics. Two specific models of the dependence of a female's fitness on her number of matings are considered: in model 1, female fitness decreases linearly with increasing number of matings and in model 2, there is an optimal number of matings that maximizes female fitness. For each of these models, we obtain the conditions for a coevolutionary process to establish costly male and female traits and examine under what circumstances polymorphism is maintained at equilibrium. Then we discuss how assumptions in previous models of sexual conflict are translated to fit to our model framework and compare our results with those of the previous studies. The simplicity of our models allows us to consider sexual conflict in various contexts within a single framework. In addition, we find that our model 2 shows more complicated evolutionary dynamics than model 1. In particular, the population exhibits bistability, where the evolutionary outcome depends on the initial state, only in model 2.     

Genetic differentiation by sexual conflict

Sexual conflict has been suggested as a general cause of genetic diversification in reproductive characters, and as a possible cause of speciation. We use individual-based simulations to study the dynamics of sexual conflict in an isolated diploid population with no spatial structure. To explore the effects of genetic details, we consider two different types of interlocus interaction between female and male traits, and three different types of intra-locus interaction. In the simulations, sexual conflict resulted in at least the following five regimes: (1) continuous coevolutionary chase, (2) evolution toward an equilibrium, (3) cyclic coevolution, (4) extensive genetic differentiation in female traits/genes only, and (5) extensive genetic differentiation in both male and female traits/genes. Genetic differentiation was hardly observed when the traits involved in reproduction were determined additively and interacted in a trait-by-trait way. When the traits interacted in a component-by-component way, genetic differentiation was frequently observed under relatively broad conditions. The likelihood of genetic differentiation largely depended on the number of loci and the type of within-locus dominance. With multiple loci per trait, genetic differentiation was often observed but sympatric speciation was typically hindered by recombination. Sympatric speciation was possible but only under restrictive conditions. Our simulations also highlight the importance of stochastic effects in the dynamics of sexual conflict.     

Intralocus sexual conflict diminishes the benefits of sexual selection

Evolution based on the benefits of acquiring “good genes” in sexual selection is only plausible with the reliable transmission of genetic quality from one generation to the next. Accumulating evidence suggests that sexually antagonistic (SA) genes with opposite effects on Darwinian fitness when expressed in the two different sexes may be common in animals and plants. These SA genes should weaken the potential indirect genetic benefits of sexual selection by reducing the fitness of opposite-sex progeny from high-fitness parents. Here we use hemiclonal analysis in the fruit fly, Drosophila melanogaster, to directly measure the inheritance of fitness across generations, over the entire genome. We show that any potential genetic benefits of sexual selection in this system are not merely weakened, but completely reversed over one generation because high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons. Moreover, male fitness was not inherited by sons, consistent with both theory and recent evidence connecting this form of SA variation with the X chromosome. This inheritance pattern may help to explain how genetic variation for fitness is sustained despite strong sexual selection, and why the ZW sex chromosome system found in birds and butterflies appears to foster the evolution of extreme secondary sexual characters in males.     

Detecting sexual conflict and sexually antagonistic coevolution

We begin by providing an operational definition of sexual conflict that applies to both inter- and intralocus conflict. Using this definition, we examine a series of simple coevolutionary models to elucidate fruitful approaches for detecting interlocus sexual conflict and resultant sexually antagonistic coevolution. We then use published empirical examples to illustrate the utility of these approaches. Three relevant attributes emerge. First, the dynamics of sexually antagonistic coevolution may obscure the conflict itself. Second, competing models of inter-sexual coevolution may yield similar population patterns near equilibria. Third, a variety of evolutionary forces underlying competing models may be acting simultaneously near equilibria. One main conclusion is that studies of emergent patterns in extant populations (e.g. studies of population and/or female fitness) are unlikely to allow us to distinguish among competing coevolutionary models. Instead, we need more research aimed at identifying the forces of selection acting on shared traits and sexually antagonistic traits. More specifically, we need a greater number of functional studies of female traits as well as studies of the consequences of both male and female traits for female fitness. A mix of selection and manipulative studies on these is likely the most promising route.     

Intralocus sexual conflict and offspring sex ratio

Males and females frequently have different fitness optima for shared traits, and as a result, genotypes that are high fitness as males are low fitness as females, and vice versa. When this occurs, biasing of offspring sex-ratio to reduce the production of the lower-fitness sex would be advantageous, so that for example, broods produced by high-fitness females should contain fewer sons. We tested for offspring sex-ratio biasing consistent with these predictions in broad-horned flour beetles. We found that in both wild-type beetles and populations subject to artificial selection for high- and low-fitness males, offspring sex ratios were biased in the predicted direction: low-fitness females produced an excess of sons, whereas high-fitness females produced an excess of daughters. Thus, these beetles are able to adaptively bias sex ratio and recoup indirect fitness benefits of mate choice.     

Parental sex discrimination and intralocus sexual conflict

Intralocus sexual conflict occurs when populations segregate for alleles with opposing fitness consequences in the two sexes. This form of selection is known to be capable of maintaining genetic and fitness variation in nature, the extent of which is sensitive to the underlying genetics. We present a one-locus model of a haploid maternal effect that has sexually antagonistic consequences for offspring. The evolutionary dynamics of these maternal effects are distinct from those of haploid direct effects under sexual antagonism because the relevant genes are expressed only in females. Despite this, we find the same opportunity for sexually antagonistic polymorphism at the maternal effect locus as at a direct effect locus. Thus, sexually antagonistic maternal effects may underlie some natural genetic variation. The model we present permits alternative interpretations of how the genes are expressed and how the fitness variation is assigned, which invites a theoretical comparison to models of both imprinted genes and sex allocation.     

Intralocus sexual conflict over human height

Intralocus sexual conflict (IASC) occurs when a trait under selection in one sex constrains the other sex from achieving its sex-specific fitness optimum. Selection pressures on body size often differ between the sexes across many species, including humans: among men individuals of average height enjoy the highest reproductive success, while shorter women have the highest reproductive success. Given its high heritability, IASC over human height is likely. Using data from sibling pairs from the Wisconsin Longitudinal Study, we present evidence for IASC over height: in shorter sibling pairs (relatively) more reproductive success (number of children) was obtained through the sister than through the brother of the sibling pair. By contrast, in average height sibling pairs most reproductive success was obtained through the brother relative to the sister. In conclusion, we show that IASC over a heritable, sexually dimorphic physical trait (human height) affects Darwinian fitness in a contemporary human population.     

The conditional economics of sexual conflict

Sexual conflict is a fundamentally important aspect of male–female interactions. In this opinion piece, we emphasize two approaches that warrant significantly greater attention. First, we review the importance of understanding the ‘economics’ (costs and benefits) of sexual interactions and note surprisingly large, unrecognized gaps in our knowledge. Second, we highlight the novel obstacles and opportunities afforded by the dependence of sexually antagonistic (SA) selection on both the local environment and condition of the interacting individuals. We conclude that more research in these two areas is essential to fully understand the evolution of SA interactions and will provide significant new insights into the extent to which coevolution of the sexes is shaped by conflict. We argue that these approaches, although not new to the field, are undervalued and under-represented.     

The evolutionary outcome of sexual conflict

Inter-locus sexual conflict occurs by definition when there is sexually antagonistic selection on a trait so that the optimal trait value differs between the sexes. As a result, there is selection on each sex to manipulate the trait towards its own optimum and resist such manipulation by the other sex. Sexual conflict often leads additionally to the evolution of harmful behaviour and to self-reinforcing and even perpetual sexually antagonistic coevolution. In an attempt to understand the determinants of these different outcomes, I compare two groups of traits-those related to parental investment (PI) and to mating-over which there is sexual conflict, but which have to date been explored by largely separate research traditions. A brief review suggests that sexual conflict over PI, particularly over PI per offspring, leads less frequently to the evolution of manipulative behaviour, and rarely to the evolution of harmful behaviour or to the rapid evolutionary changes which may be symptomatic of sexually antagonistic coevolution. The chief determinants of the evolutionary outcome of sexual conflict are the benefits of manipulation and resistance, the costs of manipulation and resistance, and the feasibility of manipulation. All three of these appear to contribute to the differences in the evolutionary outcome of conflicts over PI and mating. A detailed dissection of the evolutionary changes following from sexual conflict exposes greater complexity than a simple adaptation-counter-adaptation cycle and clarifies the role of harm. Not all of the evolutionary changes that follow from sexual conflict are sexually antagonistic, and harm is not necessary for sexually antagonistic coevolution to occur. In particular, whereas selection on the trait over which there is conflict is by definition sexually antagonistic, collateral harm is usually in the interest of neither sex. This creates the opportunity for palliative adaptations which reduce collateral harm. Failure to recognize that such adaptations are in the interest of both sexes can hinder our understanding of the evolutionary outcome of sexual conflict.     

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.     

Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster, we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Sensory ecology, receiver biases and sexual selection

During courtship, signals are sent between the sexes, and received signals contain information that forms the basis of decision making. Much is known about signal content, but less is known about signal design-what makes signals work efficiently? A consideration of design not only gives new insights into the evolution of signals (including novelty), but also allows the development of specific and testable predictions about the direction of evolution. Recently there has been increased interest in signal design, but this has resulted in some apparently divergent views in the literature.     

Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.     

Receptive females mitigate costs of sexual conflict

Males typically gain fitness from multiple mating, whereas females often lose fitness from numerous mating, potentially leading to sexual conflict over mating. This conflict is expected to favour the evolution of female resistance to mating. However, females may incur male harassment if they refuse to copulate; thus, greater female resistance may increase costs imposed by males. Here, I show that the evolution of resistance to mating raises fitness disadvantages of interacting with males when mating is harmful in female adzuki bean beetles, Callosobruchus chinensis. Females that were artificially selected for higher and lower remating propensity evolved to accept and resist remating, respectively. Compared with females that evolved to accept remating, females that evolved to resist it suffered higher fitness costs from continuous exposure to males. The costs of a single mating measured by the effect on longevity did not differ among selection line females. This study indicates that receptive rather than resistant females mitigate the fitness loss resulting from sexual conflict, suggesting that even though mating is harmful, females can evolve to accept additional mating.     

Reversed sexual conflict in a promiscuous antelope

A general tenet of sexual conflict theory is that males have higher optimum mating rates than do females and therefore should be more persistent when it comes to mating. However, in promiscuous species, females might benefit from high mating rates as a result of increased conception probability with favored males, whereas favored males benefit from mating selectively because of sperm depletion. When this results in higher optimum mating rates for females than for males, there is potential for reversed sexual conflicts between persistent females and resistant males. Here I report evidence of such a reversed sexual conflict in a promiscuous antelope, the African topi. Rather than mating randomly, favored males prefer to balance mating investment equally between females as predicted by strategic sperm allocation theory. Females, however, enhance their probability of mating with favored males through aggression toward mating pairs. Supporting the idea that aggressive females thereby harass males to mate at a rate that is suboptimal from the males' perspective, males become increasingly likely to counterattack aggressive females with whom they have already mated disproportionately, and such male counterattacks are associated with refusal to mate with the aggressive females. This study points to reversed sexual conflict as a more significant evolutionary force in promiscuous mammals than previously thought; however, such conflicts probably often go unnoticed because males, in contrast to females, can avoid mating without conspicuous resistance.     

Intralocus sexual conflict resolved through gene duplication

Gene duplication is mainly recognized by its primary role in the origin of new genes and functions. However, the idea that gene duplication can be a central player in resolving sexual genetic conflicts through its potential to generate sex-biased and sex-specifically expressed genes, has been almost entirely overlooked. We review recent data and theory that support gene duplication as a theoretically predicted and experimentally supported means of resolving intralocus sexual antagonism. We believe that this role is probably the consequence of sexual conflict for housekeeping genes that are required in males and females, and which are expressed in sexually dimorphic tissues (i.e. where sexually antagonistic selection is exerted). We think that these genes cannot evolve tissue-specific expression unless they duplicate.