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.     

Cross‐sex genetic correlations and the evolution of sex‐specific local adaptation: Insights from classical trait clines in Drosophila melanogaster

Natural selection varies widely among locations of a species’ range, favoring population divergence and adaptation to local environmental conditions. Selection also differs between females and males, favoring the evolution of sexual dimorphism. Both forms of within‐species evolutionary diversification are widely studied, though largely in isolation, and it remains unclear whether environmental variability typically generates similar or distinct patterns of selection on each sex. Studies of sex‐specific local adaptation are also challenging because they must account for genetic correlations between female and male traits, which may lead to correlated patterns of trait divergence between sexes, whether or not local selection patterns are aligned or differ between the sexes. We quantified sex‐specific divergence in five clinally variable traits in Drosophila melanogaster that individually vary in their magnitude of cross‐sex genetic correlation (i.e., from moderate to strongly positive). In all five traits, we observed parallel male and female clines, regardless of the magnitude of their genetic correlation. These patterns imply that parallel spatial divergence of female and male traits is a reflection of sexually concordant directional selection imposed by local environmental conditions. In such contexts, genetic correlations between the sexes promote, rather than constrain, local adaptation to a spatially variable environment.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

Evolutionary inevitability of sexual antagonism

Sexual antagonism, whereby mutations are favourable in one sex and disfavourable in the other, is common in natural populations, yet the root causes of sexual antagonism are rarely considered in evolutionary theories of adaptation. Here, we explore the evolutionary consequences of sex-differential selection and genotype-by-sex interactions for adaptation in species with separate sexes. We show that sexual antagonism emerges naturally from sex differences in the direction of selection on phenotypes expressed by both sexes or from sex-by-genotype interactions affecting the expression of such phenotypes. Moreover, modest sex differences in selection or genotype-by-sex effects profoundly influence the long-term evolutionary trajectories of populations with separate sexes, as these conditions trigger the evolution of strong sexual antagonism as a by-product of adaptively driven evolutionary change. The theory demonstrates that sexual antagonism is an inescapable by-product of adaptation in species with separate sexes, whether or not selection favours evolutionary divergence between males and females.     

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.”     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Genetic correlations and sex‐specific adaptation in changing environments

Females and males have conflicting evolutionary interests. Selection favors the evolution of different phenotypes within each sex, yet divergence between the sexes is constrained by the shared genetic basis of female and male traits. Current theory predicts that such “sexual antagonism” should be common: manifesting rapidly during the process of adaptation, and slow in its resolution. However, these predictions apply in temporally stable environments. Environmental change has been shown empirically to realign the direction of selection acting on shared traits and thereby alleviate signals of sexually antagonistic selection. Yet there remains no theory for how common sexual antagonism should be in changing environments. Here, we analyze models of sex‐specific evolutionary divergence under directional and cyclic environmental change, and consider the impact of genetic correlations on long‐run patterns of sex‐specific adaptation. We find that environmental change often aligns directional selection between the sexes, even when they have divergent phenotypic optima. Nevertheless, some forms of environmental change generate persistent sexually antagonistic selection that is difficult to resolve. Our results reinforce recent empirical observations that changing environmental conditions alleviate conflict between males and females. They also generate new predictions regarding the scope for sexually antagonistic selection and its resolution in changing environments.     

Sexual dimorphism in the tusked frog, Adelotus brevis (Anura:Myobatrachidae): the roles of natural and sexual selection

At least two adaptive processes can lead to the evolution of sexual dimorphism: sexual selection (e.g. male-male combat) or natural selection (e.g. dietary divergence). We investigated the adaptive significance of a distinctive pattern of sexual dimorphism in a south-eastern Australian frog, Adelotus brevis. Male Adelotus grow larger than female conspecifics, have larger heads relative to body size, and have large paired projections (‘tusks’) in the lower jaw. All of these traits are rare among anurans. We quantified the degree of dimorphism in Adelotus, and gathered data on diets and mating systems of this species to evaluate the possible roles of sexual selection and dietary divergence in favoring die evolution of these sexually dimorphic traits. Analysis of prey items in alimentary tracts revealed significant sex differences in prey types. For example, females ate proportionally more arthropods and fewer molluscs than did males. However, this difference is likely to be a secondary consequence of habitat differences between the sexes (due in turn to their different reproductive roles) rather than a selective force for the evolution of sexual dimorphism. Calling males spend their time in moist habitats where pondsnails are abundant, whereas females are more often encountered in the drier arthropod-rich woodlands. A three-year behavioural ecology study on a field population revealed that reproductive males engage in agonistic interactions, with the sexually dimorphic tusks used to attack rivals. Larger body size contributed to male reproductive success. Small males were excluded from calling sites and, among the calling males, larger animals had higher reproductive success (numbers of matings) than did smaller individuals. Hence, the atypical pattern of sexual dimorphism in Adelotus brevis seems to have resulted from sexual selection for larger body size and tusk size in males, in the context of male-male agonistic behaviour, rather than natural selection for ecological divergence between the sexes.     

Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats

Many hypotheses, either sex‐related or environment‐related, have been proposed to explain sexual size dimorphism in birds. Two populations of blue tits provide an interesting case study for testing these hypotheses because they live in contrasting environments in continental France and in Corsica and exhibit different degree of sexual size dimorphism. Contrary to several predictions, the insular population is less dimorphic than the continental one but neither the sexual selection hypothesis nor the niche variation hypothesis explain the observed patterns. In the mainland population it is advantageous for both sexes to be large, and males are larger than females. In Corsica, however, reproductive success was greater for pairs in which the male was relatively small, i.e. pairs in which sexual size dimorphism is reduced. The most likely explanation is that interpopulation differences in sexual size dimorphism are determined not by sex‐related factors, but by differences in sex‐specific reproductive roles and responses to environmental factors. Because of environmental stress on the island as a result of food shortage and high parasite infestations, the share of parents in caring for young favours small size in males so that a reduced sexual size dimorphism is not the target of selection but a by‐product of mechanisms that operate at the level of individual sexes.     

Peak shifts and extinction under sex-specific selection

A well-known property of sexual selection combined with a cross-sex genetic correlation (r_mf) is that it can facilitate a peak shift on the adaptive landscape. How do these diversifying effects of sexual selection + r_mf balance with the constraints imposed by such sexual antagonism, to affect the macroevolution of sexual dimorphism? Here, I extend existing quantitative genetic models of evolution on complex adaptive landscapes. Beyond recovering classical predictions for the conditions promoting a peak shift, I show that when r_mf is moderate to strong, relatively weak sexual selection is required to induce a peak shift in males only. Increasing the strength of sexual selection leads to a sexually concordant peak shift, suggesting that macroevolutionary rates of sexual dimorphism may be largely decoupled from the strength of within-population sexual selection. Accounting explicitly for demography further reveals that sex-specific peak shifts may be more likely to be successful than concordant shifts in the face of extinction, especially when natural selection is strong. An overarching conclusion is that macroevolutionary patterns of sexual dimorphism are unlikely to be readily explained by within-population estimates of selection or constraint alone.     

Sexual dimorphism in relation to current selection in the house finch

Abstract.— Sexual dimorphism is thought to have evolved in response to selection pressures that differ between males and females. Our aim in this study was to determine the role of current net selection in shaping and maintaining contemporary sexual dimorphism in a recently established population of the house finch ( Carpodacus mexicanus ) in Montana. We found strong differences between sexes in direction of selection on sexually dimorphic traits, significant heritabilities of these traits, and a close congruence between current selection and observed sexual dimorphism in Montana house finches. Strong directional selection on sexually dimorphic traits and similar intensities of selection in each sex suggested that sexual dimorphism arises from adaptive responses in males and females, with both sexes being far from their local fitness optimum. This pattern is expected when a recently established population experiences continuous immigration from ecologically distinct areas of a species range or as a result of widely fluctuating selection pressures, as found in our study. Strong and sexually dimorphic selection pressures on heritable morphological traits, in combination with low phenotypic and genetic covariation among these traits during growth, may have accounted for close congruence between current selection and observed sexual dimorphism in the house finch. This conclusion is consistent with the profound adaptive population divergence in sexual dimorphism that accompanied very successful colonization of most of the North America by the house finch over the last 50 years.     

Sexual size dimorphism and selection in the wild in the waterstrider Aquarius remigis: Body size,components of body size and male mating success

Sexual size dimorphism is assumed to be adaptive and is expected to evolve in response to a difference in the net selection pressures on the sexes. Although a demonstration of sexual selection is neither necessary nor sufficient to explain the evolution of sexual size dimorphism, sexual selection is generally assumed to be a major evolutionary force. If contemporary sexual selection is important in the evolution and maintenance of sexual size dimorphism then we expect to see concordance between patterns of sexual selection and patterns of sexual dimorphism. We examined sexual selection in the wild, acting on male body size, and components of body size, in the waterstrider Aquarius remigis, as part of a long term study examining net selection pressures on the two sexes in this species. Selection was estimated on both a daily and annual basis. Since our measure of fitness (mating success) was behavioral, we estimated reliabilities to determine if males perform consistently. Reliabilities were measured as ? statistics and range from fair to perfect agreement with substantial agreement overall. We found significant univariate sexual selection favoring larger total length in the first year of our study but not in the second. Multivariate analysis of components of body size revealed that sexual selection for larger males was not acting directly on total length but on genital length. Sexual selection for larger male body size was opposed by direct selection favoring smaller midfemoral lengths. While males of this species are smaller than females, they have longer genital segments and wider forefemora. Patterns of contemporary sexual selection and sexual size dimorphism agree only for genital length. For total length, and all other components of body size examined, contemporary sexual selection was either nonsignificant or opposed the pattern of size dimporhism. Thus, while the net pressures of contemporary selection for the species may still act to maintain sexual size dimorphism, sexual selection alone does not.     

Sexual selection,sexual dimorphism and plant phylogeny

Summary Darwin examined sexual dimorphism in animals, arguing that sexual selection was important in the evolution of such dimorphism. Sexual dimorphism in plants may have parallel causes and costs.The processes that contribute to sexual dimorphism may also lead to speciation and morphological differences among related species, as argued originally by Darwin. Where sexes are separate and dimorphism is well-developed, males of related animal species (both vertebrate and invertebrate) are often strikingly different from each other, while females may be virtually indistinguishable. A similar pattern may exist in plants: it is frequently the males (of dioecious taxa) or the male portions of the flower (in co-sexual flowers) that apparently have diversified. I suggest that the similarity of pattern may be accounted for by a similarity of process.In addition, sexual selection may have contributed to certain evolutionary trends within the angiosperms and, indeed, to angiosperm radiation.     

Sexual dimorphism and adaptive speciation: two sides of the same ecological coin

Models of adaptive speciation are typically concerned with demonstrating that it is possible for ecologically driven disruptive selection to lead to the evolution of assortative mating and hence speciation. However, disruptive selection could also lead to other forms of evolutionary diversification, including ecological sexual dimorphisms. Using a model of frequency-dependent intraspecific competition, we show analytically that adaptive speciation and dimorphism require identical ecological conditions. Numerical simulations of individual-based models show that a single ecological model can produce either evolutionary outcome, depending on the genetic independence of male and female traits and the potential strength of assortative mating. Speciation is inhibited when the genetic basis of male and female ecological traits allows the sexes to diverge substantially. This is because sexual dimorphism, which can evolve quickly, can eliminate the frequency-dependent disruptive selection that would have provided the impetus for speciation. Conversely, populations with strong assortative mating based on ecological traits are less likely to evolve a sexual dimorphism because females cannot simultaneously prefer males more similar to themselves while still allowing the males to diverge. This conflict between speciation and dimorphism can be circumvented in two ways. First, we find a novel form of speciation via negative assortative mating, leading to two dimorphic daughter species. Second, if assortative mating is based on a neutral marker trait, trophic dimorphism and speciation by positive assortative mating can occur simultaneously. We conclude that while adaptive speciation and ecological sexual dimorphism may occur simultaneously, allowing for sexual dimorphism restricts the likelihood of adaptive speciation. Thus, it is important to recognize that disruptive selection due to frequency-dependent interactions can lead to more than one form of adaptive splitting.     

HOMAGE TO BATEMAN: SEX ROLES PREDICT SEX DIFFERENCES IN SEXUAL SELECTION

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role‐reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role‐reversed species compared to species with conventional sex roles. Variance‐based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait‐based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.     

GENETIC DRIFT IN ANTAGONISTIC GENES LEADS TO DIVERGENCE IN SEX‐SPECIFIC FITNESS BETWEEN EXPERIMENTAL POPULATIONS OF DROSOPHILA MELANOGASTER

Males and females differ in their reproductive roles and as a consequence are often under diverging selection pressures on shared phenotypic traits. Theory predicts that divergent selection can favor the invasion of sexually antagonistic alleles, which increase the fitness of one sex at the detriment of the other. Sexual antagonism can be subsequently resolved through the evolution of sex‐specific gene expression, allowing the sexes to diverge phenotypically. Although sexual dimorphism is very common, recent evidence also shows that antagonistic genetic variation continues to segregate in populations of many organisms. Here we present empirical data on the interaction between sexual antagonism and genetic drift in populations that have independently evolved under standardized conditions. We demonstrate that small experimental populations of Drosophila melanogaster have diverged in male and female fitness, with some populations showing high male, but low female fitness while other populations show the reverse pattern. The between‐population patterns are consistent with the differentiation in reproductive fitness being driven by genetic drift in sexually antagonistic alleles. We discuss the implications of our results with respect to the maintenance of antagonistic variation in subdivided populations and consider the wider implications of drift in fitness‐related genes.     

Partitioning of resources: the evolutionary genetics of sexual conflict over resource acquisition and allocation

Fitness depends on both the resources that individuals acquire and the allocation of those resources to traits that influence survival and reproduction. Optimal resource allocation differs between females and males as a consequence of their fundamentally different reproductive strategies. However, because most traits have a common genetic basis between the sexes, conflicting selection between the sexes over resource allocation can constrain the evolution of optimal allocation within each sex, and generate trade‐offs for fitness between them (i.e. ‘sexual antagonism’ or ‘intralocus sexual conflict’). The theory of resource acquisition and allocation provides an influential framework for linking genetic variation in acquisition and allocation to empirical evidence of trade‐offs between distinct life‐history traits. However, these models have not considered the emergence of trade‐offs within the context of sexual dimorphism, where they are expected to be particularly common. Here, we extend acquisition–allocation theory and develop a quantitative genetic framework for predicting genetically based trade‐offs between life‐history traits within sexes and between female and male fitness. Our models demonstrate that empirically measurable evidence of sexually antagonistic fitness variation should depend upon three interacting factors that may vary between populations: (1) the genetic variances and between‐sex covariances for resource acquisition and allocation traits, (2) condition‐dependent expression of resource allocation traits and (3) sex differences in selection on the allocation of resource to different fitness components.     

The evolution of sexual size dimorphism in the house finch. II. Population divergence in relation to local selection

Recent colonization of ecologically distinct areas in North America by the house finch (Carpodacus mexicanus) was accompanied by strong population divergence in sexual size dimorphism. Here we examined whether this divergence was produced by population differences in local selection pressures acting on each sex. In a long-term study of recently established populations in Alabama, Michigan, and Montana, we examined three selection episodes for each sex: selection for pairing success, overwinter survival, and within-season fecundity. Populations varied in intensity of these selection episodes, the contribution of each episode to the net selection, and in the targets of selection. Direction and intensity of selection strongly differed between sexes, and different selection episodes often favored opposite changes in morphological traits. In each population, current net selection for sexual dimorphism was highly concordant with observed sexual dimorphism--in each population, selection for dimorphism was the strongest on the most dimorphic traits. Strong directional selection on sexually dimorphic traits, and similar intensities of selection in both sexes, suggest that in each of the recently established populations, both males and females are far from their local fitness optimum, and that sexual dimorphism has arisen from adaptive responses in both sexes. Population differences in patterns of selection on dimorphism, combined with both low levels of ontogenetic integration in heritable sexually dimorphic traits and sexual dimorphism in growth patterns, may account for the close correspondence between dimorphism in selection and observed dimorphism in morphology across house finch populations.     

INTRALOCUS SEXUAL CONFLICT OVER IMMUNE DEFENSE,GENDER LOAD,AND SEX‐SPECIFIC SIGNALING IN A NATURAL LIZARD POPULATION

In species with separate sexes, antagonistic selection on males and females (intralocus sexual conflict) can result in a gender load that can be resolved through the evolution of sexual dimorphism. We present data on intralocus sexual conflict over immune defense in a natural population of free‐ranging lizards (Uta stansburiana) and discuss the resolution of this conflict. Intralocus sexual conflict arises from correlational selection between immune defense and orange throat coloration in these lizards. Males with orange throats and high antibody responses had enhanced survival, but the same trait combination reduced female fitness. This sexual antagonism persisted across the life cycle and was concordant between the juvenile and adult life stages. The opposing selective pressure on males and females is ameliorated by a negative intersexual genetic correlation (r_m,f=?0.86) for immune defense. Throat coloration was also genetically correlated with immune defense, but the sign of this genetic correlation differed between the sexes. This resulted in sex‐specific signaling of immunological condition. We also found evidence for a sex‐specific maternal effect on sons with potential to additionally reduce the gender load. These results have implications for signaling evolution, genetic integration between adaptive traits, sex allocation, and mutual mate choice for indirect fitness benefits.