The dynamics of sexually antagonistic coevolution and the complex influences of mating system and genetic correlation

Sexual conflict has been proposed to be a mediator of speciation but recent theoretical work, as well as empirical studies, suggests that sexual conflict may also be able to prevent speciation and to preserve genetic polymorphism within a species. Here, we develop a population genetic model and study the effects of sexual conflict in a polymorphic population. The morphs mate assortatively based on different sexually antagonistic traits and females are assumed to suffer a cost when the proportion of matching males is high. We consider the model in two different mating systems; promiscuity and polygyny. Our results show that genetic polymorphism may be maintained through negative frequency dependent selection established by assortative mating and female conflict costs. However, the outcome significantly differs between mating systems. Furthermore, we show that indirect selection may have profound effects on the evolutionary dynamics of a sexual conflict.     

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.     

Independent evolution of the sexes promotes amphibian diversification

Classic ecological theory predicts that the evolution of sexual dimorphism constrains diversification by limiting morphospace available for speciation. Alternatively, sexual selection may lead to the evolution of reproductive isolation and increased diversification. We test contrasting predictions of these hypotheses by examining the relationship between sexual dimorphism and diversification in amphibians. Our analysis shows that the evolution of sexual size dimorphism (SSD) is associated with increased diversification and speciation, contrary to the ecological theory. Further, this result is unlikely to be explained by traditional sexual selection models because variation in amphibian SSD is unlikely to be driven entirely by sexual selection. We suggest that relaxing a central assumption of classic ecological models—that the sexes share a common adaptive landscape—leads to the alternative hypothesis that independent evolution of the sexes may promote diversification. Once the constraints of sexual conflict are relaxed, the sexes can explore morphospace that would otherwise be inaccessible. Consistent with this novel hypothesis, the evolution of SSD in amphibians is associated with reduced current extinction threat status, and an historical reduction in extinction rate. Our work reconciles conflicting predictions from ecological and evolutionary theory and illustrates that the ability of the sexes to evolve independently is associated with a spectacular vertebrate radiation.     

CORRELATED EVOLUTION OF SEXUAL DIMORPHISM AND MALE DIMORPHISM IN A CLADE OF NEOTROPICAL HARVESTMEN

Secondary sexual traits increase male fitness, but may be maladaptive in females, generating intralocus sexual conflict that is ameliorated through sexual dimorphism. Sexual selection on males may also lead some males to avoid expenditure on secondary sexual traits and achieve copulations using alternative reproductive tactics (ARTs). Secondary sexual traits can increase or decrease fitness in males, depending on which ART they employ, generating intralocus tactical conflict that can be ameliorated through male dimorphism. Due to the evolutionary forces acting against intralocus sexual and tactical conflicts, male dimorphism could coevolve with sexual dimorphism, a hypothesis that we tested by investigating these dimorphisms across 48 harvestman species. Using three independently derived phylogenies, we consistently found that the evolution of sexual dimorphism was correlated with that of male dimorphism, and suggest that the major force behind this relationship is the similarity between selection against intralocus sexual conflict and selection against intralocus tactical conflict. We also found that transitions in male dimorphism were more likely in the presence of sexual dimorphism, indicating that if a sexually selected trait arises on an autosome and is expressed in both sexes, its suppression in females probably evolves earlier than its suppression in small males that adopt ARTs.     

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 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.     

SEXUAL SELECTION IS INVOLVED IN SPECIATION IN A LAND SNAIL RADIATION ON CRETE

We investigated the importance of sexual selection in facilitating speciation in a land snail radiation on Crete. We used differences in the genitalia of the Cretan Xerocrassa species as potential indices of sexual selection. First, we rejected the hypothesis that differences in the genitalia of the Xerocrassa species can be explained by genetic drift using coalescent simulations based on a mitochondrial gene tree. Second, we showed that there is no evidence for the hypothesis that the differences in the genitalia can be explained by natural selection against hybrids under the assumption that this is more likely in geographically overlapping species pairs and clades. Third, we showed that there is a positive scaling between male spermatophore-producing organs and female spermatophore-receiving organs indicating sexual coevolution. The spermatophore enables the sperm to escape from the female gametolytic organ. Thus, the coevolution might be a consequence of sexual conflict or cryptic female choice. Finally, we showed that the evolution of differences in the length of the flagellum that forms the tail of the spermatophore is concentrated toward the tips of the tree indicating that it is involved in speciation. If speciation is facilitated by sexual selection, niches may remain conserved and nonadaptive radiation may result.     

Darwin's ‘mystery of mysteries’: the role of sexual selection in plant speciation

Sexual selection is considered one of the key processes that contribute to the emergence of new species. While the connection between sexual selection and speciation has been supported by comparative studies, the mechanisms that mediate this connection remain unresolved, especially in plants. Similarly, it is not clear how speciation processes within plant populations translate into large-scale speciation dynamics. Here, we review the mechanisms through which sexual selection, pollination, and mate choice unfold and interact, and how they may ultimately produce reproductive isolation in plants. We also overview reproductive strategies that might influence sexual selection in plants and illustrate how functional traits might connect speciation at the population level (population differentiation, evolution of reproductive barriers; i.e. microevolution) with evolution above the species level (macroevolution). We also identify outstanding questions in the field, and suitable data and tools for their resolution. Altogether, this effort motivates further research focused on plants, which might potentially broaden our general understanding of speciation by sexual selection, a major concept in evolutionary biology.     

PERSPECTIVE: CHASE-AWAY SEXUAL SELECTION: ANTAGONISTIC SEDUCTION VERSUS RESISTANCE

A model of sexual selection that leads to the evolution of exaggerated male display characters that is based on antagonistic coevolution between the sexes is described. The model is motivated by three lines of research: intersexual conflict with respect to mating, sensory exploitation, and the evolution of female resistance, as opposed to preference, for male display traits. The model generates unique predictions that permit its operation to be distinguished from other established models of sexual selection. One striking prediction is that females will frequently win the coevolutionary arms race with males, leaving them encumbered with costly ornaments that have little value except that their absence understimulates females. Examples from the literature suggest that the model may have broad application in nature. The chase-away model is a special case of the more general phenomenon of Interlocus Contest Evolution (ICE).     

Linking color polymorphism maintenance and speciation

Here, we review the recently burgeoning literature on color polymorphisms, seeking to integrate studies of the maintenance of genetic variation and the evolution of reproductive isolation. Our survey reveals that several mechanisms, some operating between populations and others within them, can contribute to both color polymorphism persistence and speciation. As expected, divergent selection clearly can couple with gene flow to maintain color polymorphism and mediate speciation. More surprisingly, recent evidence suggests that diverse forms of within-population sexual selection can generate negative frequency dependence and initiate reproductive isolation. These findings deserve additional study, particularly concerning the roles of heterogeneous visual environments and correlational selection. Finally, comparative studies and more comprehensive approaches are required to elucidate when color polymorphism evolves, persists, or leads to speciation.     

Speciation and Sexual Conflict

We review mathematical models that explicitly consider the dynamics of evolutionary change driven by sexual conflict over mating rate when males are selected for increasing mating success whereas females are selected to restrict mating rate. These models focus on a pair of traits each of which is controlled by a separate set of genes expressed in one sex only. The traits control the probability of mating and/or fertilization. Overall, there are at least six different dynamic regimes observed in models of sexual conflict: (1) continuous coevolutionary chase between the sexes (which can result in allopatric speciation as a byproduct), (2) evolution towards an equilibrium, (3) cyclic evolution, (4) evolution towards a line of equilibria with subsequent random drift along this line, (5) Buridan’s Ass regime involving extensive diversification in female alleles without comparable diversification in male alleles, and (6) extensive diversification in both male and female alleles (which can result in sympatric speciation). Mathematical models also show that different dynamic regimes can be observed with the same set of parameter values but under different initial conditions. It is also possible that the same population switches from one regime to another as a result of stochastic perturbations due to, say, random genetic drift. Moreover, different sets of loci controlling mating and fertilization in the same species can follow different dynamic regimes. We attempt to make some generalizations and identify important directions for theoretical and empirical work.     

The risk of polyspermy in three congeneric sea urchins and its implications for gametic incompatibility and reproductive isolation

Developmental failure caused by excess sperm (polyspermy) is thought to be an important mechanism driving the evolution of gamete-recognition proteins, reproductive isolation, and speciation in marine organisms. However, these theories assume that there is heritable variation in the susceptibility to polyspermy and that this variation is related to the overall affinity between sperm and eggs. These assumptions have not been critically examined. We investigated the relationship between ease of fertilization and susceptibility to polyspermy within and among three congeneric sea urchins. The results from laboratory studies indicate that, both within and among species, individuals and species that produce eggs capable of fertilization at relatively low sperm concentrations are more susceptible to polyspermy, whereas individuals and species producing eggs that require higher concentrations of sperm to be fertilized are more resistant to polyspermy. This relationship sets the stage for selection on gamete traits that depend on sperm availability and for sexual conflict that can influence the evolution of gamete-recognition proteins and eventually lead to reproductive isolation.     

Engines of speciation: a comparative study in birds of prey

Sexual selection as a promoter of speciation has received much attention in recent years, but has produced highly equivocal evidence. Here, I test whether sexual conflict is related to species richness among genera in accipitrid birds of prey using phylogenetically controlled comparative analyses. Increased species richness was associated with both 'male-win' as well as 'female-win' situations, i.e. males being able to promote gene flow through mating or females being able to restrict gene flow through female choice. Species richness was higher when plumage differed between males and females and in polygynous breeding systems compared with monogamous ones. To assess the relative importance of sexual conflict and natural selection as correlates of species richness simultaneously, I also performed a multivariate analysis of correlates of species richness. Population density, plumage polymorphism, geographic range size and breeding latitude were predictors of species richness for birds of prey. These results stress the importance of both sexual and natural selection in determining species richness but with a clear overall emphasis on natural selection in birds of prey.     

THE ROLE OF MULTILEVEL SELECTION IN THE EVOLUTION OF SEXUAL CONFLICT IN THE WATER STRIDER AQUARIUS REMIGIS

In evolution, exploitative strategies often create a paradox in which the most successful individual strategy “within” the group is also the most detrimental strategy “for” the group, potentially resulting in extinction. With regard to sexual conflict, the overexploitation of females by harmful males can yield similar consequences. Despite these evolutionary implications, little research has addressed why sexual conflict does not ultimately drive populations to extinction. One possibility is that groups experiencing less sexual conflict are more productive than groups with greater conflict. However, most studies of sexual conflict are conducted in a single isolated group, disregarding the potential for selection among groups. We observed Aquarius remigis water striders in a naturalistic multigroup pool in which individuals could freely disperse among groups. The free movement of individuals generated variation in aggression and sex‐ratio among groups, thereby increasing the importance of between‐group selection compared to within‐group selection. Females dispersed away from local aggression, creating more favorable mating environments for less‐aggressive males. Furthermore, the use of contextual analysis revealed that individual male aggression positively predicted fitness whereas aggression at the group level negatively predicted fitness, empirically demonstrating the conflict between levels of selection acting on mating aggression.     

Unusual modes of reproduction in social insects: shedding light on the evolutionary paradox of sex

The study of alternative genetic systems and mixed modes of reproduction, whereby sexual and asexual reproduction is combined within the same lifecycle, is of fundamental importance as they may shed light on classical evolutionary issues, such as the paradox of sex. Recently, several such cases were discovered in social insects. A closer examination of these systems has revealed many amazing facts, including the mixed use of asexual and sexual reproduction for the production of new queens and workers, males that can clone themselves and the routine use of incest without deleterious genetic consequences. In addition, in several species, remarkable cases of asexually reproducing socially parasitic worker lineages have been discovered. The study of these unusual systems promises to provide insight into many basic evolutionary questions, including the maintenance of sex, the expression of sexual conflict and kin conflict and the evolution of cheating in asexual lineages.     

Does reproductive isolation evolve faster in larger populations via sexually antagonistic coevolution?

Sexual conflict over reproductive investment can lead to sexually antagonistic coevolution and reproductive isolation. It has been suggested that, unlike most models of allopatric speciation, the evolution of reproductive isolation through sexually antagonistic coevolution will occur faster in large populations as these harbour greater levels of standing genetic variation, receive larger numbers of mutations and experience more intense sexual selection. We tested this in bruchid beetle populations (Callosobruchus maculatus) by manipulating population size and standing genetic variability in replicated lines derived from founders that had been released from sexual conflict for 90 generations. We found that after 19 generations of reintroduced sexual conflict, none of our treatments had evolved significant overall reproductive isolation among replicate lines. However, as predicted, measures of reproductive isolation tended to be greater among larger populations. We discuss our methodology, arguing that reproductive isolation is best examined by performing a matrix of allopatric and sympatric crosses whereas measurement of divergence requires crosses with a tester line.     

Sex allocation and sexual conflict in simultaneously hermaphroditic animals

Links between sex allocation (SA) and sexual conflict in simultaneous hermaphrodites have been evident since Charnov''s landmark paper published 30 years ago. We discuss two links, namely the potential for sexual conflict over SA between sperm donor and recipient, and the importance of post-copulatory sexual selection and the resulting sexual conflict for the evolution of SA. We cover the little empirical and theoretical work exploring these links, and present an experimental test of one theoretical prediction. The link between SA and sexual conflict is an interesting field for future empirical and theoretical research.     

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.     

Intersexual ontogenetic conflict

Evolutionary conflict has been investigated at many levels of organization, from interactions between loci within a genome to the coevolution of species. Here we review evidence for intersexual ontogenetic conflict, a type of conflict that has received relatively little attention both theoretically and empirically. It is manifest during development when expression of the same allele, on average, moves one sex towards, and the other sex away from, its phenotypic optimum. We first introduce this type of conflict with an illustrative example and assess conditions for maintaining polymorphism for alleles underlying the conflict. We then summarize evidence from our own experiments with Drosophila melanogaster that show substantial genome‐wide sexually antagonistic fitness variation. Finally we discuss evidence from other organisms and some of the ramifications of widespread polymorphism for sexually antagonistic fitness variation.     

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.