The B-matrix harbors significant and sex-specific constraints on the evolution of multicharacter sexual dimorphism

The extent to which sexual dimorphism can evolve within a population depends on an interaction between sexually divergent selection and constraints imposed by a genetic architecture that is shared between males and females. The degree of constraint within a population is normally inferred from the intersexual genetic correlation, r(mf) . However, such bivariate correlations ignore the potential constraining effect of genetic covariances between other sexually coexpressed traits. Using the fruit fly Drosophila serrata, a species that exhibits mutual mate preference for blends of homologous contact pheromones, we tested the impact of between-sex between-trait genetic covariances using an extended version of the genetic variance-covariance matrix, G, that includes Lande's (1980) between-sex covariance matrix, B. We find that including B greatly reduces the degree to which male and female traits are predicted to diverge in the face of divergent phenotypic selection. However, the degree to which B alters the response to selection differs between the sexes. The overall rate of male trait evolution is predicted to decline, but its direction remains relatively unchanged, whereas the opposite is found for females. We emphasize the importance of considering the B-matrix in microevolutionary studies of constraint on the evolution of sexual dimorphism.     

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.     

Elimination of a genetic correlation between the sexes via artificial correlational selection

Genetic correlations between the sexes can constrain the evolution of sexual dimorphism and be difficult to alter, because traits common to both sexes share the same genetic underpinnings. We tested whether artificial correlational selection favoring specific combinations of male and female traits within families could change the strength of a very high between-sex genetic correlation for flower size in the dioecious plant Silene latifolia. This novel selection dramatically reduced the correlation in two of three selection lines in fewer than five generations. Subsequent selection only on females in a line characterized by a lower between-sex genetic correlation led to a significantly lower correlated response in males, confirming the potential evolutionary impact of the reduced correlation. Although between-sex genetic correlations can potentially constrain the evolution of sexual dimorphism, our findings reveal that these constraints come not from a simple conflict between an inflexible genetic architecture and a pattern of selection working in opposition to it, but rather a complex relationship between a changeable correlation and a form of selection that promotes it. In other words, the form of selection on males and females that leads to sexual dimorphism may also promote the genetic phenomenon that limits 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.     

Genetic variation and covariation in floral allocation of two species of Schiedea with contrasting levels of sexual dimorphism

The evolution of sexual dimorphism depends in part on the additive genetic variance-covariance matrices within females, within males, and across the sexes. We investigated quantitative genetics of floral biomass allocation in females and hermaphrodites of gynodioecious Schiedea adamantis (Caryophyllaceae). The G-matrices within females (G(f)), within hermaphrodites (G(m)), and between sexes (B) were compared to those for the closely related S. salicaria, which exhibits a lower frequency of females and less-pronounced sexual dimorphism. Additive genetic variation was detected in all measured traits in S. adamantis, with narrow-sense heritability from 0.34-1.0. Female allocation and floral size traits covaried more tightly than did those traits with allocation to stamens. Between-sex genetic correlations were all <1, indicating sex-specific expression of genes. Common principal-components analysis detected differences between G(f) and G(m) , suggesting potential for further independent evolution of the sexes. The two species of Schiedea differed in G(m) and especially so in G(f) , with S. adamantis showing greater genetic variation in capsule mass and tighter genetic covariation between female allocation traits and flower size in females. Despite greater sexual dimorphism in S. adamantis, genetic correlations between the two sexes (standardized elements of B) were similar to correlations between sexes in S. salicaria.     

Selection in a fluctuating environment and the evolution of sexual dimorphism in the seed beetle Callosobruchus maculatus

Temperature changes in the environment, which realistically include environmental fluctuations, can create both plastic and evolutionary responses of traits. Sexes might differ in either or both of these responses for homologous traits, which in turn has consequences for sexual dimorphism and its evolution. Here, we investigate both immediate changes in and the evolution of sexual dimorphism in response to a changing environment (with and without fluctuations) using the seed beetle Callosobruchus maculatus. We investigate sex differences in plasticity and also the genetic architecture of body mass and developmental time dimorphism to test two existing hypotheses on sex differences in plasticity (adaptive canalization hypothesis and condition dependence hypothesis). We found a decreased sexual size dimorphism in higher temperature and that females responded more plastically than males, supporting the condition dependence hypothesis. However, selection in a fluctuating environment altered sex-specific patterns of genetic and environmental variation, indicating support for the adaptive canalization hypothesis. Genetic correlations between sexes (r(MF) ) were affected by fluctuating selection, suggesting facilitated independent evolution of the sexes. Thus, the selective past of a population is highly important for the understanding of the evolutionary dynamics of sexual dimorphism.     

Genetic constraints and the evolution of display trait sexual dimorphism by natural and sexual selection

The evolution of sexual dimorphism involves an interaction between sex-specific selection and a breakdown of genetic constraints that arise because the two sexes share a genome. We examined genetic constraints and the effect of sex-specific selection on a suite of sexually dimorphic display traits in Drosophila serrata. Sexual dimorphism varied among nine natural populations covering a substantial portion of the species range. Quantitative genetic analyses showed that intersexual genetic correlations were high because of autosomal genetic variance but that the inclusion of X-linked effects reduced genetic correlations substantially, indicating that sex linkage may be an important mechanism by which intersexual genetic constraints are reduced in this species. We then explored the potential for both natural and sexual selection to influence these traits, using a 12-generation laboratory experiment in which we altered the opportunities for each process as flies adapted to a novel environment. Sexual dimorphism evolved, with natural selection reducing sexual dimorphism, whereas sexual selection tended to increase it overall. To this extent, our results are consistent with the hypothesis that sexual selection favors evolutionary divergence of the sexes. However, sex-specific responses to natural and sexual selection contrasted with the classic model because sexual selection affected females rather than males.     

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.     

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.     

Phenotypic divergence and inter-specific trait correlation in a plant-pollinator/seed predator mutualism

Plant-pollinator interactions have been suggested as key drivers of morphological divergence and speciation of the involved taxa. These interactions can also promote sexual dimorphism in both the plant and pollinator, particularly if the pollinator is also a seed-eater and/or exerts different selection pressures on male and female plants. Here we tested the hypotheses that plant-pollinator interactions can be reflected in trait variation and sexual dimorphism in both organisms within and across populations. Across nine European populations, we examined intraspecific variation and sexual dimorphism in phenotypic traits potentially involved in the plant–insect interaction of the dioecious white campion Silene latifolia (Caryophyllaceae) and its specialist pollinator Hadena bicruris (Noctuidae). This interaction is expected to entail sex-specific selective pressures, as female moths lay eggs on female plants and the larvae predate on the seeds during their development. We compared divergence in phenotypic traits among populations and between sexes within populations, examined correlations between plant and pollinator traits, and between phenotypic distances and genetic distances among co-occurring populations for both plants and insects. We found key differences in phenotypic traits across populations of both the plant and moth, though only in the moth were these differences correlated with geographic distances. We also found evidence for sexual dimorphism in the plant but not in the pollinator. Evolution of floral sexual dimorphism in S. latifolia most likely results from the joint contribution of different selective forces, including biotic interactions with H. bicruris moths.     

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.     

Sexual dimorphism in the baboon facial skeleton

Baboons exhibit marked sexual dimorphism in many aspects of their morphology. Dimorphism is especially pronounced in the face. We use finite-element analysis to investigate the ontogeny of sexual dimorphism in a cross-sectional sample of baboon (Papio sp.) faces. This method provides detailed quantitative information about size and shape changes at anatomical landmarks in the face during growth. Allometric results suggest that sexual dimorphism in facial size and shape is produced by ontogenetic scaling: males and females share a common ontogenetic trajectory. Analyses of growth in time, which complement allometric analyses, show that female growth slows much earlier than male growth, accounting for the differences between sexes. Local size and local shape follow similar patterns of growth, but changes in these variables are slower in females. Local and global facial size are much more dimorphic than local and global facial shape.     

Signal trait sexual dimorphism and mutual sexual selection in Drosophila serrata

Abstract The evolution of sexual dimorphism may occur when natural and sexual selection result in different optimum trait values for males and females. Perhaps the most prominent examples of sexual dimorphism occur in sexually selected traits, for which males usually display exaggerated trait levels, while females may show reduced expression of the trait. In some species, females also exhibit secondary sexual traits that may either be a consequence of a correlated response to sexual selection on males or direct sexual selection for female secondary sexual traits. In this experiment, we simultaneously measure the intersex genetic correlations and the relative strength of sexual selection on males and females for a set of cuticular hydrocarbons in Drosophila serrata . There was significant directional sexual selection on both male and female cuticular hydrocarbons: the strength of sexual selection did not differ among the sexes but males and females preferred different cuticular hydrocarbons. In contrast with many previous studies of sexual dimorphism, intersex genetic correlations were low. The evolution of sexual dimorphism in D. serrata appears to have been achieved by sex-limited expression of traits controlled by genes on the X chromosome and is likely to be in its final stages.     

Sex‐specific plasticity and genotype × sex interactions for age and size of maturity in the sheepshead swordtail,Xiphophorus birchmanni

Responses to sexually antagonistic selection are thought to be constrained by the shared genetic architecture of homologous male and female traits. Accordingly, adaptive sexual dimorphism depends on mechanisms such as genotype‐by‐sex interaction (G×S) and sex‐specific plasticity to alleviate this constraint. We tested these mechanisms in a population of Xiphophorus birchmanni (sheepshead swordtail), where the intensity of male competition is expected to mediate intersexual conflict over age and size at maturity. Combining quantitative genetics with density manipulations and analysis of sex ratio variation, we confirm that maturation traits are dimorphic and heritable, but also subject to large G×S. Although cross‐sex genetic correlations are close to zero, suggesting sex‐linked genes with important effects on growth and maturation are likely segregating in this population, we found less evidence of sex‐specific adaptive plasticity. At high density, there was a weak trend towards later and smaller maturation in both sexes. Effects of sex ratio were stronger and putatively adaptive in males but not in females. Males delay maturation in the presence of mature rivals, resulting in larger adult size with subsequent benefit to competitive ability. However, females also delay maturation in male‐biased groups, incurring a loss of reproductive lifespan without apparent benefit. Thus, in highly competitive environments, female fitness may be limited by the lack of sex‐specific plasticity. More generally, assuming that selection does act antagonistically on male and female maturation traits in the wild, our results demonstrate that genetic architecture of homologous traits can ease a major constraint on the evolution of adaptive dimorphism.     

THE GENOMIC ARCHITECTURE OF SEXUAL DIMORPHISM IN THE DIOECIOUS PLANT SILENE LATIFOLIA

Evaluating the genetic architecture of sexual dimorphism can aid our understanding of the extent to which shared genetic control of trait variation versus sex‐specific control impacts the evolutionary dynamics of phenotypic change within each sex. We performed a QTL analysis on Silene latifolia to evaluate the contribution of sex‐specific QTL to phenotypic variation in 46 traits, whether traits involved in trade‐offs had colocalized QTL, and whether the distribution of sex‐specific loci can explain differences between the sexes in their variance/covariance matrices. We used a backcross generation derived from two artificial‐selection lines. We found that sex‐specific QTL explained a significantly greater percent of the variation in sexually dimorphic traits than loci expressed in both sexes. Genetically correlated traits often had colocalized QTL, whose signs were in the expected direction. Lastly, traits with different genetic correlations within the sexes displayed a disproportionately high number of sex‐specific QTL, and more QTL co‐occurred in males than females, suggesting greater trait integration. These results show that sex differences in QTL patterns are congruent with theory on the resolution of sexual conflict and differences based on G ‐matrix results. They also suggest that trade‐offs and trait integration are likely to affect males more than females.     

Genetic architecture of sexual dimorphism in a subdioecious plant with a proto-sex chromosome

The rise of sexual dimorphism is thought to coincide with the evolution of sex chromosomes. Yet because sex chromosomes in many species are ancient, we lack empirical evidence of the earliest stages of this transition. We use QTL analysis to examine the genetic architecture of sexual dimorphism in subdioecious octoploid Fragaria virginiana. We demonstrate that the region housing the male-function locus controls the majority of quantitative variation in proportion fruit set, confirming the existence of a proto-sex chromosome, and houses major QTL for eight additional sexually dimorphic traits, consistent with theory and data from animals and plants with more advanced sex chromosomes. We also detected autosomal QTL, demonstrating contributions to phenotypic variation in sexually dimorphic traits outside the sex-determining region. Moreover, for proportion seed set we found significant epistatic interactions between autosomal QTL and the male-function locus, indicating sex-limited QTL. We identified linked QTL reflecting trade-offs between male and female traits expected from theory and positive integration of male traits. These findings indicate the potential for the evolution of greater sexual dimorphism. Involvement of linkage groups homeologous to the proto-sex chromosome in these correlations reflects the polyploid origin of F. virginiana and raises the possibility that chromosomes in this homeologous group were predisposed to become the sex chromosome.     

Quantitative Genetics of Drosophila Melanogaster. II. Heritabilities and Genetic Correlations between Sexes for Head and Thorax Traits

A quantitative genetic analysis is reported for traits on the head and thorax of adult fruit flies, Drosophila melanogaster. Females are larger than males, and the magnitude of sexual dimorphism is similar for traits derived from the same imaginal disc, but the level of sexual dimorphism varies widely across discs. The greatest difference between males and females occurs for the dimensions of the sclerotized mouthparts of the proboscis. Most of the traits studied are highly heritable with heritabilities ranging from 0.26 to 0.84 for males and 0.27 to 0.81 for females. In general, heritabilities are slightly higher for males, possibly reflecting the effect of dosage compensation on X-linked variance. The X chromosome contributes substantially to variance for many of these traits, and including results reported elsewhere, the variance for over two-thirds of the traits studied includes X-linked variance. The genetic correlations between sexes for the same trait are generally high and close to unity. Coupled with the small differences in the traits between sexes for heritabilities and phenotypic variances, these results suggest that selection would be very slow to change the level of sexual dimorphism in size of various body parts.     

Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia

Many species exhibit sexual dimorphism in a variety of characters, and the underlying genetic architecture of dimorphism potentially involves sex-specific differences in the additive-genetic variance-covariance matrix (G) of dimorphic traits. We investigated the quantitative-genetic structure of dimorphic traits in the dioecious plant Silene latifolia by estimating G (including within-sex matrices, G(m), G(f), and the between-sex variance-covariance matrix, B), and the phenotypic variance-covariance matrix (P) for seven traits. Flower number was the most sexually dimorphic trait, and was significantly genetically correlated with all traits within each sex. Negative genetic correlations between flower size and number suggested a genetic trade-off in investment, but positive environmental correlations between the same traits resulted in no physical evidence for a trade-off in the phenotype. Between-sex genetic covariances for homologous traits were always greater than 0 but smaller than 1, showing that some, but not all, of the variation in traits is caused by genes or alleles with sex-limited expression. Using common principal-components analysis (CPCA), a maximum-likelihood (ML) estimation approach, and element-by-element comparison to compare matrices, we found that G(m) and G(f) differed significantly in eigenstructure because of dissimilarity in covariances involving leaf traits, suggesting the presence of variation in sex-limited genes with pleiotropic effects and/or linkage between sex-limited loci. The sex-specific structure of G is expected to cause differences in the correlated responses to selection within each sex, promoting the further evolution and maintenance of dimorphism.     

Genetic differences among populations in sexual dimorphism: evidence for selection on males in a dioecious plant

Genetic variation among populations in the degree of sexual dimorphism may be a consequence of selection on one or both sexes. We analysed genetic parameters from crosses involving three populations of the dioecious plant Silene latifolia, which exhibits sexual dimorphism in flower size, to determine whether population differentiation was a result of selection on one or both sexes. We took the novel approach of comparing the ratio of population differentiation of a quantitative trait (Q(ST) ) to that of neutral genetic markers (F(ST) ) for males vs. females. We attributed 72.6% of calyx width variation in males to differences among populations vs. only 6.9% in females. The Q(ST) /F(ST) ratio was 4.2 for males vs. 0.4 for females, suggesting that selection on males is responsible for differentiation among populations in calyx width and its degree of sexual dimorphism. This selection may be indirect via genetic correlations with other morphological and physiological traits.