SEX CHROMOSOME LINKED GENETIC VARIANCE AND THE EVOLUTION OF SEXUAL DIMORPHISM OF QUANTITATIVE TRAITS

Theory predicts that sex chromsome linkage should reduce intersexual genetic correlations thereby allowing the evolution of sexual dimorphism. Empirical evidence for sex linkage has come largely from crosses and few studies have examined how sexual dimorphism and sex linkage are related within outbred populations. Here, we use data on an array of different traits measured on over 10,000 individuals from two pedigreed populations of birds (collared flycatcher and zebra finch) to estimate the amount of sex‐linked genetic variance (h²_z). Of 17 traits examined, eight showed a nonzero h²_Z estimate but only four were significantly different from zero (wing patch size and tarsus length in collared flycatchers, wing length and beak color in zebra finches). We further tested how sexual dimorphism and the mode of selection operating on the trait relate to the proportion of sex‐linked genetic variance. Sexually selected traits did not show higher h²_Z than morphological traits and there was only a weak positive relationship between h²_Z and sexual dimorphism. However, given the relative scarcity of empirical studies, it is premature to make conclusions about the role of sex chromosome linkage in the evolution of sexual dimorphism.     

Multivariate genetic architecture of the Anolis dewlap reveals both shared and sex‐specific features of a sexually dimorphic ornament

Darwin viewed the ornamentation of females as an indirect consequence of sexual selection on males and the transmission of male phenotypes to females via the ‘laws of inheritance’. Although a number of studies have supported this view by demonstrating substantial between‐sex genetic covariance for ornament expression, the majority of this work has focused on avian plumage. Moreover, few studies have considered the genetic basis of ornaments from a multivariate perspective, which may be crucial for understanding the evolution of sex differences in general, and of complex ornaments in particular. Here, we provide a multivariate, quantitative‐genetic analysis of a sexually dimorphic ornament that has figured prominently in studies of sexual selection: the brightly coloured dewlap of Anolis lizards. Using data from a paternal half‐sibling breeding experiment in brown anoles (Anolis sagrei), we show that multiple aspects of dewlap size and colour exhibit significant heritability and a genetic variance–covariance structure ( G ) that is broadly similar in males ( G _m) and females ( G _f). Whereas sexually monomorphic aspects of the dewlap, such as hue, exhibit significant between‐sex genetic correlations (r_mf), sexually dimorphic features, such as area and brightness, exhibit reduced r_mf values that do not differ from zero. Using a modified random skewers analysis, we show that the between‐sex genetic variance–covariance matrix ( B) should not strongly constrain the independent responses of males and females to sexually antagonistic selection. Our microevolutionary analysis is in broad agreement with macroevolutionary perspectives indicating considerable scope for the independent evolution of coloration and ornamentation in males and females.     

INTRALOCUS SEXUAL CONFLICT AND ENVIRONMENTAL STRESS

Intralocus sexual conflict (IaSC) occurs when selection at a given locus favors different alleles in males and females, placing a fundamental constraint on adaptation. However, the relative impact of IaSC on adaptation may become reduced in stressful environments that expose conditionally deleterious mutations to selection. The genetic correlation for fitness between males and females (r_MF) provides a quantification of IaSC across the genome. We compared IaSC at a benign (29°C) and a stressful (36°C) temperature by estimating r_MFs in two natural populations of the seed beetle Callosobruchus maculatus using isofemale lines. In one population, we found substantial IaSC under benign conditions signified by a negative r_MF (?0.51) and, as predicted, a significant reduction of IaSC under stress signified by a reversed and positive r_MF (0.21). The other population displayed low IaSC at both temperatures (r_MF: 0.38; 0.40). In both populations, isofemale lines harboring alleles beneficial to males but detrimental to females at benign conditions tended to show overall low fitness under stress. These results offer support for low IaSC under stress and suggest that environmentally sensitive and conditionally deleterious alleles that are sexually selected in males mediate changes in IaSC. We discuss implications for adaptive evolution in sexually reproducing populations.     

Resistance to oxidative stress shows low heritability and high common environmental variance in a wild bird

Oxidative stress was recently demonstrated to affect several fitness‐related traits and is now well recognized to shape animal life‐history evolution. However, very little is known about how much resistance to oxidative stress is determined by genetic and environmental effects and hence about its potential for evolution, especially in wild populations. In addition, our knowledge of phenotypic sexual dimorphism and cross‐sex genetic correlations in resistance to oxidative stress remains extremely limited despite important evolutionary implications. In free‐living great tits (Parus major), we quantified heritability, common environmental effect, sexual dimorphism and cross‐sex genetic correlation in offspring resistance to oxidative stress by performing a split‐nest cross‐fostering experiment where 155 broods were split, and all siblings (n = 791) translocated and raised in two other nests. Resistance to oxidative stress was measured as both oxidative damage to lipids and erythrocyte resistance to a controlled free‐radical attack. Both measurements of oxidative stress showed low additive genetic variances, high common environmental effects and phenotypic sexual dimorphism with males showing a higher resistance to oxidative stress. Cross‐sex genetic correlations were not different from unity, and we found no substantial heritability in resistance to oxidative stress at adult age measured on 39 individuals that recruited the subsequent year. Our study shows that individual ability to resist to oxidative stress is primarily influenced by the common environment and has a low heritability with a consequent low potential for evolution, at least at an early stage of life.     

Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Cross‐sex genetic covariances limit the evolvability of wing‐shape within and among species of Drosophila

The independent evolution of males and females is potentially constrained by both sexes inheriting the same alleles from their parents. This genetic constraint can limit the evolvability of complex traits; however, there are few studies of multivariate evolution that incorporate cross‐sex genetic covariances in their predictions. Drosophila wing‐shape has emerged as a model high‐dimensional phenotype; wing‐shape is highly evolvable in contemporary populations, and yet perplexingly stable across phylogenetic timescales. Here, we show that cross‐sex covariances in Drosophila melanogaster, given by the B ‐matrix, may considerably bias wing‐shape evolution. Using random skewers, we show that B would constrain the response to antagonistic selection by 90%, on average, but would double the response to concordant selection. Both cross‐sex within‐trait and cross‐sex cross‐trait covariances determined the predicted response to antagonistic selection, but only cross‐sex within‐trait covariances facilitated the predicted response to concordant selection. Similar patterns were observed in the direction of extant sexual dimorphism in D. melanogaster, and in directions of most and least dimorphic variation across the Drosophila phylogeny. Our results highlight the importance of considering between‐sex genetic covariances when making predictions about evolution on both macro‐ and microevolutionary timescales, and may provide one more explanatory piece in the puzzle of stasis.     

Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Sexual differences in locomotor performance in Tropidurus catalanensis lizards (Squamata: Tropiduridae) – body shape,size and limb musculature explain variation between males and females

Sexual dimorphism (SD) is the evolutionary outcome of selection acting differently on males and females. Several studies describe sexual differences in body size, although other morphological traits might be allometric between sexes and imply functional consequences. Here we test whether morphological differences between sexes in size and shape in the lizard Tropidurus catalanensis explain variation in performance of four locomotor traits. Our results show that males are larger than females and also exhibit longer limbs, longer muscles and larger muscle cross‐sectional areas, while females have longer trunks and more sharped anterior claws; males outperform females in all locomotor performances measured. Sexual differences in sprinting and climbing is related with body size, and climbing performance is also explained by limb lengths, by differences in lengths and cross‐sectional areas of specific muscles, and by interlimb distances. Between‐sex differences in exertion are also related to SD, despite associations with sharper posterior claws that are independent of sex. Grasping performance, however, is associated with some muscle and morphological parameters that are not sexually dimorphic. Together our results suggest that morphology might be under sexual selection in T. catalanensis, given that better locomotor performance likely favours male lizards in typical activities of this polygenic species, such as territory defence and female acquisition. Moreover, the longer trunks that characterize females may confer more space to accommodate eggs. On the other hand, territory defence by males probably increases their exposure to predators, resulting in a synergistic effect of sexual and natural selection in the evolution of SD in T. catalanensis.     

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.     

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.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Incorporating an ontogenetic perspective into evolutionary theory of sexual size dimorphism

Sexual size dimorphism (SSD) describes divergent body sizes of adult males and females. While SSD has traditionally been explained by sexual and fecundity selection, recent advances in physiology and developmental biology emphasize that SSD would occur proximately because of sexual differences in ontogenetic growth trajectories (i.e., growth rate and duration). Notably, these ontogenetic traits are subject to energetic or time constraints and thus traded off with fitness components (e.g., survival and reproduction). To elucidate the importance of such ontogenetic trade‐offs in the evolution of SSD, we developed a new theoretical framework by extending quantitative genetic models for the evolution of sexual dimorphism in which we reinterpret the trait as body size and reformulate sex‐specific fitness in size‐dependent manners. More specifically, we assume that higher growth rate or longer growth duration leads to larger body size and higher reproductive success but incurs the cost of lower survivorship or shorter reproduction period. We illustrate how two sexes would optimize ontogenetic growth trajectories in sex‐specific ways and exhibit divergent body sizes. The present framework provides new insights into the evolutionary theory of SSD and predictions for empirical testing.     

THE EVOLUTIONARY STABILITY OF CROSS‐SEX,CROSS‐TRAIT GENETIC COVARIANCES

Although knowledge of the selective agents behind the evolution of sexual dimorphism has advanced considerably in recent years, we still lack a clear understanding of the evolutionary durability of cross‐sex genetic covariances that often constrain its evolution. We tested the relative stability of cross‐sex genetic covariances for a suite of homologous contact pheromones of the fruit fly Drosophila serrata, along a latitudinal gradient where these traits have diverged in mean. Using a Bayesian framework, which allowed us to account for uncertainty in all parameter estimates, we compared divergence in the total amount and orientation of genetic variance across populations, finding divergence in orientation but not total variance. We then statistically compared orientation divergence of within‐sex ( G ) to cross‐sex ( B ) covariance matrices. In line with a previous theoretical prediction, we find that the cross‐sex covariance matrix, B , is more variable than either within‐sex G matrix. Decomposition of B matrices into their symmetrical and nonsymmetrical components revealed that instability is linked to the degree of asymmetry. We also find that the degree of asymmetry correlates with latitude suggesting a role for spatially varying natural selection in shaping genetic constraints on the evolution of sexual dimorphism.     

Insights into the genetic architecture of sexual dimorphism from an interspecific cross between two diverging Silene (Caryophyllaceae) species

The evolution of sexual dimorphism in species with separate sexes is influenced by the resolution of sexual conflicts creating sex differences through genetic linkage or sex‐biased expression. Plants with different degrees of sexual dimorphism are thus ideal to study the genetic basis of sexual dimorphism. In this study we explore the genetic architecture of sexual dimorphism between Silene latifolia and Silene dioica. These species have chromosomal sex determination and differ in the extent of sexual dimorphism. To test whether QTL for sexually dimorphic traits have accumulated on the sex chromosomes and to quantify their contribution to species differences, we create a linkage map and performed QTL analysis of life history, flower and vegetative traits using an unidirectional interspecific F2 hybrid cross. We found support for an accumulation of QTL on the sex chromosomes and that sex differences explained a large proportion of the variance between species, suggesting that both natural and sexual selection contributed to species divergence. Sexually dimorphic traits that also differed between species displayed transgressive segregation. We observed a reversal in sexual dimorphism in the F2 population, where males tended to be larger than females, indicating that sexual dimorphism is constrained within populations but not in recombinant hybrids. This study contributes to the understanding of the genetic basis of sexual dimorphism and its evolution in Silene.     

Little evidence for intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction in the black field cricket Teleogryllus commodus

There is often large divergence in the effects of key nutrients on life span (LS) and reproduction in the sexes, yet nutrient intake is regulated in the same way in males and females given dietary choice. This suggests that the sexes are constrained from feeding to their sex‐specific nutritional optima for these traits. Here, we examine the potential for intralocus sexual conflict (IASC) over optimal protein and carbohydrate intake for LS and reproduction to constrain the evolution of sex‐specific nutrient regulation in the field cricket, Teleogryllus commodus. We show clear sex differences in the effects of protein and carbohydrate intake on LS and reproduction and strong positive genetic correlations between the sexes for the regulated intake of these nutrients. However, the between‐sex additive genetic covariance matrix had very little effect on the predicted evolutionary response of nutrient regulation in the sexes. Thus, IASC appears unlikely to act as an evolutionary constraint on sex‐specific nutrient regulation in T. commodus. This finding is supported by clear sexual dimorphism in the regulated intake of these nutrients under dietary choice. However, nutrient regulation did not coincide with the nutritional optima for LS or reproduction in either sex, suggesting that IASC is not completely resolved in T. commodus.     

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.     

Self‐fertilization and inbreeding limit the scope for sexually antagonistic polymorphism

Sexual antagonism occurs when there is a positive intersexual genetic correlation in trait expression but opposite fitness effects of the trait(s) in males and females. As such, it constrains the evolution of sexual dimorphism and may therefore have implications for adaptive evolution. There is currently considerable evidence for the existence of sexually antagonistic genetic variation in laboratory and natural populations, but how sexual antagonism interacts with other evolutionary phenomena is still poorly understood in many cases. Here, we explore how self‐fertilization and inbreeding affect the maintenance of polymorphism for sexually antagonistic loci. We expected a priori that selfing should reduce the region of polymorphism, as inbreeding reduces the frequency of heterozygotes and speeds fixation. This expectation was supported, but although previous results suggest that the more an allele that is deleterious to one sex is dominant in that sex, the smaller the region of parameter space that will admit polymorphism, we found that this effect is weakened by self‐fertilization. However, the effect of inbreeding is not strong enough to completely cancel out the effect of dominance: For a given frequency of inbreeding, it will still be the case that the more dominant the alleles are in their deleterious context, the smaller the region of parameter space in which they can exist at polymorphism.     

Evolution of stickleback feeding behaviour: genetics of population divergence at different ontogenetic stages

The evolutionary significance of individual consistency in a given behaviour – called animal personality – has been subject to a lot of recent research. However, the genetic underpinnings of population divergence in mean personality have rarely been studied, especially across different ontogenetic stages. Previous work has shown that marine vs. pond populations of nine‐spined sticklebacks (Pungitius pungitius) have undergone adaptive divergence in a series of fitness‐related traits, including behaviour. One particular behavioural trait important in this system is feeding activity: giant pond sticklebacks are more active feeders than their normal sized marine conspecifics. In a common garden experiment, we raised individuals from pure and hybrid F₁‐generation crosses of a highly divergent marine – pond population pair to see if (i) feeding activity and/or its ontogenetic change was consistent between individuals, and if (ii) population divergence at different ontogenetic stages could be explained by additive genetic, nonadditive genetic or maternal effects. We found that feeding activity decreased with age, but that these changes were consistently different among both individuals and crosses. The among cross patterns were consistent with a nonadditive genetic scenario: in the early period pond sticklebacks expressed dominance for high feeding activity, while in the late period marine sticklebacks expressed dominance for low feeding activity. We conclude that nine‐spined sticklebacks exhibit different feeding personalities, and that the population divergence in feeding personality is explainable by age‐dependent expression of genetic dominance.     

Evolution of sexually dimorphic pheromone profiles coincides with increased number of male‐specific chemosensory organs in Drosophila prolongata

Binary communication systems that involve sex‐specific signaling and sex‐specific signal perception play a key role in sexual selection and in the evolution of sexually dimorphic traits. The driving forces and genetic changes underlying such traits can be investigated in systems where sex‐specific signaling and perception have emerged recently and show evidence of potential coevolution. A promising model is found in Drosophila prolongata, which exhibits a species‐specific increase in the number of male chemosensory bristles. We show that this transition coincides with recent evolutionary changes in cuticular hydrocarbon (CHC) profiles. Long‐chain CHCs that are sexually monomorphic in the closest relatives of D. prolongata (D. rhopaloa, D. carrolli, D. kurseongensis, and D. fuyamai) are strongly male‐biased in this species. We also identify an intraspecific female‐limited polymorphism, where some females have male‐like CHC profiles. Both the origin of sexually dimorphic CHC profiles and the female‐limited polymorphism in D. prolongata involve changes in the relative amounts of three mono‐alkene homologs, 9‐tricosene, 9‐pentacosene, and 9‐heptacosene, all of which share a common biosynthetic origin and point to a potentially simple genetic change underlying these traits. Our results suggest that pheromone synthesis may have coevolved with chemosensory perception and open the way for reconstructing the origin of sexual dimorphism in this communication system.