A multivariate view of the evolution of sexual dimorphism

Sexual differences are often dramatic and widespread across taxa. Their extravagance and ubiquity can be puzzling because the common underlying genome of males and females is expected to impede rather than foster phenotypic divergence. Widespread dimorphism, despite a shared genome, may be more readily explained by considering the multivariate, rather than univariate, framework governing the evolution of sexual dimorphism. In the univariate formulation, differences in genetic variances and a low intersexual genetic correlation () can facilitate the evolution of sexual dimorphism. However, studies that have analysed sex‐specific differences in heritabilities or genetic variances do not always find significant differences. Furthermore, many of the reported estimates of are very high and positive. When monomorphic heritabilities and a high are present together, the evolution of sexual dimorphism on a trait‐by‐trait basis is severely constrained. By contrast, the multivariate formulation has greater generality and more flexibility. Although the number of multivariate sexual dimorphism studies is low, almost all support sex‐specific differences in the G (variance‐covariance) matrix; G matrices can differ with respect to size and/or orientation, affecting the response to selection differently between the sexes. Second, whereas positive values of the univariate quantity only hinder positive changes in sexual dimorphism, positive covariances in the intersexual covariance B matrix can either help or hinder. Similarly, the handful of studies reporting B matrices indicate that it is often asymmetric, so that B can affect the evolution of single traits differently between the sexes. Multivariate approaches typically demonstrate that genetic covariances among traits can strongly constrain trait evolution when compared with univariate approaches. By contrast, in the evolution of sexual dimorphism, a multivariate view potentially reveals more opportunities for sexual dimorphism to evolve by considering the effect sex‐specific selection has on sex‐specific G matrices and an asymmetric B matrix.     

Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

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.     

Evolution of sexual dimorphism in phenotypic covariance structure in Phymata

Sexual dimorphism is a consequence of both sex‐specific selection and potential constraints imposed by a shared genetic architecture underlying sexually homologous traits. However, genetic architecture is expected to evolve to mitigate these constraints, allowing the sexes to approach their respective optimal mean phenotype. In addition, sex‐specific selection is expected to generate sexual dimorphism of trait covariance structure (e.g., the phenotypic covariance matrix, P ), but previous empirical work has not fully addressed this prediction. We compared patterns of phenotypic divergence, for three traits in seven taxa in the insect genus Phymata (Reduviidae), to ask whether sexual dimorphism in P is common and whether its magnitude relates to the extent of sexual dimorphism in trait means. We found that sexual dimorphism in both mean and covariance structure was pervasive but also that the multivariate distance between sex‐specific means was correlated with sex differences in the leading eigenvector of P , while accounting for uncertainty in phylogenetic relationships. Collectively, our findings suggest that sexual dimorphism in covariance structure may be a common but underappreciated feature of dioecious populations.     

Sexual dimorphism explains residual variance around the survival‐reproduction tradeoff in lizards: Implications for sexual conflict over life‐history evolution*

The tradeoff between survival and reproduction is a central feature of life‐history variation, but few studies have sought to explain why females of some species exhibit relatively lower survival than expected for a given level of reproductive effort (RE). Intralocus sexual conflict theory proposes that sex differences in selection on survival and RE may, by virtue of shared genes underlying these components of fitness, prevent females from optimizing this life‐history tradeoff. To test this hypothesis, we used a phylogenetically based comparative analysis of published estimates for mean annual survival and RE from females of 82 lizard species to (1) characterize the tradeoff between survival and reproduction and (2) test whether variation around this tradeoff is explained by sexual size dimorphism (SSD), a potential proxy for sexual conflict over life‐history traits. Across species, we found a strong negative correlation between mean annual survival and RE, confirming this classic life‐history tradeoff. Although residual variance around this tradeoff is unrelated to the absolute magnitude of SSD, it is strongly related to the direction of SSD. Specifically, we found that females have lower survival than expected for a given level of RE in female‐larger species, whereas they have higher survival than expected in male‐larger species. Given that female‐larger SSD is thought to reflect selection for increased fecundity, our results suggest that intralocus sexual conflict may be particularly likely to constrain female life‐history evolution in situations where increased RE is favored, but the phenotypes that facilitate this increase (e.g., body size) are constrained by antagonistic selection on males.     

Sex-limited mutations and the evolution of sexual dimorphism

Abstract.— Although the developmental and genetic mechanisms underlying sex differences are being elucidated in great detail in a number of species, there remains a breach between proximate and evolutionary studies of sexual dimorphism. More precisely, the evolution of sex-limited gene expression at autosomal loci has not been well reasoned using either theoretical or empirical methods. Here, I show that a Mendelian genetic model including elementary details of sexual differentiation provides novel insight into the evolution of sex differences via sex limitation. This model indicates that the nature of allelic effects and the pattern of selection must be known in both sexes to predict the evolution of sex differences. That is, selection interacts with genetic variation for sexual dimorphism to produce unanticipated patterns of trait divergence or convergence between the sexes. Ultimately, this model may explain why previous models for the evolution of sexual dimorphism do not predict the erratic behavior of the sex difference during artificial selection experiments.     

The ontogeny of cross‐sex genetic correlations: an analysis of patterns

The independent evolution of males and females is typically constrained by shared genetic variance. Despite substantial research, we still know little about the evolution of cross‐sex genetic covariance and its standardized measure, the cross‐sex genetic correlation (r_MF). In particular, it is unclear if r_MF tend to vary with age. We compiled 28 traits for which ontogenetic trends in r_MF were documented. Decreases in r_MF with age were observed significantly more often than increases and the mean effect size for the relationship between r_MF and age was large and negative. This suggests that sexual dimorphism (SD) may typically evolve more readily for phenotypes expressed later in ontogeny and that evolutionary inferences related to the evolution of SD should be limited to the ontogenetic stage at which r_MF was estimated. Knowledge about ontogenetic variation in r_MF should help improving our understanding of evolutionary patterns related to SD and the resolution of intralocus sexual conflicts.     

Predicting the evolution of sexual size dimorphism

11 , Evolution 34 : 292–305) equations for predicting the evolution of sexual size dimorphism (SSD) through frequency‐dependent sexual selection, and frequency‐independent natural selection, were tested against results obtained from a stochastic genetic simulation model. The SSD evolved faster than predicted, due to temporary increases in the genetic variance brought about by directional selection. Predictions for the magnitude of SSD at equilibrium were very accurate for weak sexual selection. With stronger sexual selection the total response was greater than predicted. Large changes in SSD can occur without significant long‐term change in the genetic correlation between the sexes. Our results suggest that genetic correlations constrain both the short‐term and long‐term evolution of SSD less than predicted by the Lande model.     

The evolution of sexual dimorphism in the house finch. I. Population divergence in morphological covariance structure

Abstract Patterns of genetic variation and covariation strongly affect the rate and direction of evolutionary change by limiting the amount and form of genetic variation available to natural selection. We studied evolution of morphological variance-covariance structure among seven populations of house finches (Carpodacus mexicanus) with a known phylogenetic history. We examined the relationship between within- and among-population covariance structure and, in particular, tested the concordance between hierarchical changes in morphological variance-covariance structure and phylogenetic history of this species. We found that among-population morphological divergence in either males or females did not follow the within-population covariance patterns. Hierarchical patterns of similarity in morphological covariance matrices were not congruent with a priori defined historical pattern of population divergence. Both of these results point to the lack of proportionality in morphological covariance structure of finch populations, suggesting that random drift alone is unlikely to account for observed divergence. Furthermore, drift alone cannot explain the sex differences in within- and among-population covariance patterns or sex-specific patterns of evolution of covariance structure. Our results suggest that extensive among-population variation in sexual dimorphism in morphological covariance structure was produced by population differences in local selection pressures acting on each sex.     

Between‐sex genetic covariance constrains the evolution of sexual dimorphism in Drosophila melanogaster

Males and females share much of their genome, and as a result, intralocus sexual conflict is generated when selection on a shared trait differs between the sexes. This conflict can be partially or entirely resolved via the evolution of sex‐specific genetic variation that allows each sex to approach, or possibly achieve, its optimum phenotype, thereby generating sexual dimorphism. However, shared genetic variation between the sexes can impose constraints on the independent expression of a shared trait in males and females, hindering the evolution of sexual dimorphism. Here, we examine genetic constraints on the evolution of sexual dimorphism in Drosophila melanogaster cuticular hydrocarbon (CHC) expression. We use the extended G matrix, which includes the between‐sex genetic covariances that constitute the B matrix, to compare genetic constraints on two sets of CHC traits that differ in the extent of their sexual dimorphism. We find significant genetic constraints on the evolution of further dimorphism in the least dimorphic traits, but no such constraints for the most dimorphic traits. We also show that the genetic constraints on the least dimorphic CHCs are asymmetrical between the sexes. Our results suggest that there is evidence both for resolved and ongoing sexual conflict in D. melanogaster CHC profiles.     

Macroevolutionary patterns of sexual size dimorphism in copepods

Major theories compete to explain the macroevolutionary trends observed in sexual size dimorphism (SSD) in animals. Quantitative genetic theory suggests that the sex under historically stronger directional selection will exhibit greater interspecific variance in size, with covariation between allometric slopes (male to female size) and the strength of SSD across clades. Rensch''s rule (RR) also suggests a correlation, but one in which males are always the more size variant sex. Examining free-living pelagic and parasitic Copepoda, we test these competing predictions. Females are commonly the larger sex in copepod species. Comparing clades that vary by four orders of magnitude in their degree of dimorphism, we show that isometry is widespread. As such we find no support for either RR or for covariation between allometry and SSD. Our results suggest that selection on both sexes has been equally important. We next test the prediction that variation in the degree of SSD is related to the adult sex ratio. As males become relatively less abundant, it has been hypothesized that this will lead to a reduction in both inter-male competition and male size. However, the lack of such a correlation across diverse free-living pelagic families of copepods provides no support for this hypothesis. By comparison, in sea lice of the family Caligidae, there is some qualitative support of the hypothesis, males may suffer elevated mortality when they leave the host and rove for sedentary females, and their female-biased SSD is greater than in many free-living families. However, other parasitic copepods which do not appear to have obvious differences in sex-based mate searching risks also show similar or even more extreme SSD, therefore suggesting other factors can drive the observed extremes.     

Sex differences in the genetic architecture of aggressiveness in a sexually dimorphic spider

Sex differences in the genetic architecture of behavioral traits can offer critical insight into the processes of sex‐specific selection and sexual conflict dynamics. Here, we assess genetic variances and cross‐sex genetic correlations of two personality traits, aggression and activity, in a sexually size‐dimorphic spider, Nuctenea umbratica. Using a quantitative genetic approach, we show that both traits are heritable. Males have higher heritability estimates for aggressiveness compared to females, whereas the coefficient of additive genetic variation and evolvability did not differ between the sexes. Furthermore, we found sex differences in the coefficient of residual variance in aggressiveness with females exhibiting higher estimates. In contrast, the quantitative genetic estimates for activity suggest no significant differentiation between males and females. We interpret these results with caution as the estimates of additive genetic variances may be inflated by nonadditive genetic effects. The mean cross‐sex genetic correlations for aggression and activity were 0.5 and 0.6, respectively. Nonetheless, credible intervals of both estimates were broad, implying high uncertainty for these estimates. Future work using larger sample sizes would be needed to draw firmer conclusions on how sexual selection shapes sex differences in the genetic architecture of behavioral traits.     

Spatial variation in the temporal change of male and female melanic ornamentation in the barn owl

Because the magnitude of selection can vary between sexes and in space and time, sexually antagonistic selection is difficult to demonstrate. In a Swiss population of barn owls (Tyto alba), a heritable eumelanic colour trait (size of black spots on ventral feathers) was positively selected with respect to yearling survival only in females. It remains unclear whether the absence of negative selection in males is typical in this species. To tackle this issue indirectly, we measured the size of black spots in 1733 skin specimens collected by museums from 1816 to 2001 in seven European countries and in the Middle-East. The temporal change in spot size was sex- and country-specific. In males, spots became smaller particularly in three countries (Middle-East, Italy and Switzerland). In females, the size of spots increased significantly in two countries (UK and Spain) and decreased in two others (Germany and Switzerland). Because migration and phenotypic plasticity cannot explain these results, selection is the most likely cause. The weaker temporal change in spot size in females than males may be because of the combined effect of strong genetic correlation between the sexes and stronger negative selection in males than positive selection in females. We thus suggest that in the barn owl, spot size (or genetically correlated traits) is sexually antagonistically selected and that its pattern of selection may account for the maintenance of its variation and sexual dimorphism.     

Genetic constraints and sexual dimorphism in immune defense

The absence of continued evolutionary change despite the presence of genetic variation and directional selection is very common. Genetic correlations between traits can reduce the evolvability of traits. One intriguing example might be found in a sexual conflict over sexually dimorphic traits: a common genetic architecture constrains the response to selection on a trait subjected to sexually asymmetric selection pressures. Here we show that males and females of the mealworm beetle Tenebrio molitor differ in the quantitative genetic architecture of four traits related to immune defense and condition. Moreover, high genetic correlations between the sexes constitute a genetic constraint to the evolution of sexual dimorphism in immune defense. Our results suggest a general mechanism by which sexual conflict can promote evolutionary stasis. We furthermore show negative genetic correlations, strong indications of trade-offs, between immune traits for two pairs of traits in females.     

The evolution of sexual size dimorphism in the house finch. IV. Population divergence in ontogeny

Differences among taxa in sexual size dimorphism of adults can be produced by changes in distinct developmental processes and thus may reflect different evolutionary histories. Here we examine whether divergence in sexual dimorphism of adults between recently established Montana and Alabama populations of the house finch (Carpodacus mexicanus) can be attributed to population differences in growth of males and females. In both populations, males and females were similar at hatching, but as a result of sex-specific growth attained sexual size dimorphism by the time of independence. Timing and extent of growth varied between the sexes: Females maintained maximum rates of growth for a longer time than males, whereas males had higher initial growth rates and achieved maximum growth earlier and at smaller sizes than females. Ontogeny of sexual dimorphism differed between populations, but in each population, sexual dimorphism in growth parameters and sexual dimorphism at the time of nest leaving were similar to sexual dimorphism of adults. Variation in growth of females contributed more to population divergence than did growth of males. In each population, we found close correspondence between patterns of sexual dimorphism in growth and population divergence in morphology of adults: Traits that were the most sexually dimorphic in growth in each population contributed the most to population divergence in both sexes. We suggest that sex-specific expression of phenotypic and genetic variation throughout the ontogeny of house finches can result in different responses to selection between males and females of the same age, and thus produce fast population divergence in the sexual size dimorphism.     

Within‐population Y‐linked genetic variation for lifespan in Drosophila melanogaster

The view that the Y chromosome is of little importance for phenotypic evolution stems from early studies of Drosophila melanogaster. This species’ Y chromosome contains only 13 protein‐coding genes, is almost entirely heterochromatic and is not necessary for male viability. Population genetic theory further suggests that non‐neutral variation can only be maintained at the Y chromosome under special circumstances. Yet, recent studies suggest that the D. melanogaster Y chromosome trans‐regulates hundreds to thousands of X and autosomal genes. This finding suggests that the Y chromosome may play a far more active role in adaptive evolution than has previously been assumed. To evaluate the potential for the Y chromosome to contribute to phenotypic evolution from standing genetic variation, we test for Y‐linked variation in lifespan within a population of D. melanogaster. Assessing variation for lifespan provides a powerful test because lifespan (i) shows sexual dimorphism, which the Y is primarily predicted to contribute to, (ii) is influenced by many genes, which provides the Y with many potential regulatory targets and (iii) is sensitive to heterochromatin remodelling, a mechanism through which the Y chromosome is believed to regulate gene expression. Our results show a small but significant effect of the Y chromosome and thus suggest that the Y chromosome has the potential to respond to selection from standing genetic variation. Despite its small effect size, Y‐linked variation may still be important, in particular when evolution of sexual dimorphism is genetically constrained elsewhere in the genome.     

The evolution of sexual size dimorphism in the house finch. III. Developmental basis

Sexual size dimorphism of adults proximately results from a combination of sexually dimorphic growth patterns and selection on growing individuals. Yet, most studies of the evolution of dimorphism have focused on correlates of only adult morphologies. Here we examined the ontogeny of sexual size dimorphism in an isolated population of the house finch (Carpodacus mexicanus). Sexes differed in growth rates and growth duration; in most traits, females grew faster than males, but males grew for a longer period. Sexual dimorphism in bill traits (bill length, width, depth) and in body traits (wing, tarsus, and tail length; mass) developed during different periods of ontogeny. Growth of bill traits was most different between sexes during the juvenile period (after leaving the nest), whereas growth of body traits was most sexually dimorphic during the first few days after hatching. Postgrowth selection on juveniles strongly influenced sexual dimorphism in all traits; in some traits, this selection canceled or reversed dimorphism patterns produced by growth differences between sexes. The net result was that adult sexual dimorphism, to a large degree, was an outcome of selection for survival during juvenile stages. We suggest that previously documented fast and extensive divergence of house finch populations in sexual size dimorphism may be partially produced by distinct environmental conditions during growth in these populations.