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.     

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.     

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.     

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.     

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.     

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 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.     

Phenotypic variation and covariation indicate high evolvability of acoustic communication in crickets

Studying the genetic architecture of sexual traits provides insight into the rate and direction at which traits can respond to selection. Traits associated with few loci and limited genetic and phenotypic constraints tend to evolve at high rates typically observed for secondary sexual characters. Here, we examined the genetic architecture of song traits and female song preferences in the field crickets Gryllus rubens and Gryllus texensis. Song and preference data were collected from both species and interspecific F1 and F2 hybrids. We first analysed phenotypic variation to examine interspecific differentiation and trait distributions in parental and hybrid generations. Then, the relative contribution of additive and additive‐dominance variation was estimated. Finally, phenotypic variance–covariance ( P ) matrices were estimated to evaluate the multivariate phenotype available for selection. Song traits and preferences had unimodal trait distributions, and hybrid offspring were intermediate with respect to the parents. We uncovered additive and dominance variation in song traits and preferences. For two song traits, we found evidence for X‐linked inheritance. On the one hand, the observed genetic architecture does not suggest rapid divergence, although sex linkage may have allowed for somewhat higher evolutionary rates. On the other hand, P matrices revealed that multivariate variation in song traits aligned with major dimensions in song preferences, suggesting a strong selection response. We also found strong covariance between the main traits that are sexually selected and traits that are not directly selected by females, providing an explanation for the striking multivariate divergence in male calling songs despite limited divergence in female preferences.     

GENETIC CONSTRAINTS ON THE INDEPENDENT EVOLUTION OF MALE AND FEMALE REPRODUCTIVE CHARACTERS IN THE TRISTYLOUS PLANT LYTHRUM SALICARIA

Here we test whether the potential exists for the independent evolution of allocation to male, female, and attractive functions within a flower. We employed half-sib and parent-offspring regression methods in the tristylous plant Lythrum salicaria to determine whether there is additive genetic variation for characters important to male and female reproductive success and whether genetic correlations could constrain the independent evolution of male and female function. Although significance levels were not consistent among morph types or between populations, there were significant narrow-sense heritabilities for several traits including stamen mass, pistil mass, perianth mass, petal length, and calyx length. Traits that might be under strong stabilizing selection to promote specific pollen transfer, such as stamen and style lengths, had little heritable variation. In the majority of cases in which heritable variation was present, there were positive genetic correlations among floral traits. A strong positive genetic correlation appeared between stamen and pistil mass in the short-styled morph from one of the populations studied. This suggests that selection might not be able to act independently on biomass allocation to male and female flower parts. No evidence of negative genetic correlations appeared that would suggest trade-offs and that could augment a selection response towards sexual specialization. The observed positive correlations could be explained if we consider the “functional architecture” that underlies the covariance structure. If there is more covariance generated by pleiotropic loci controlling overall flower size than at loci controlling male versus female allocation, it could result in the observed positive covariance. At the phenotypic level, we did find significant negative partial correlations between male and female traits when flower size was controlled, but these trade-offs were among rather than within morphs.     

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.     

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 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.     

Genetic correlations do not constrain the evolution of sexual dimorphism in the moss Ceratodon purpureus

The trajectory of phenotypic evolution is constrained in the short term by genetic correlations among traits. However, the extent to which genetic correlations impose a lasting constraint is generally unknown. Here, I examine the genetic architecture of life-history variation in male and female gametophytes from two populations of the moss Ceratodon purpureus, focusing on genetic correlations within and between the sexes. A significant negative correlation between allocation to vegetative and reproductive tissue was evident in males of both populations, but not females. All traits showed between-sex correlations of significantly less than one, indicating additive genetic variance for sexual dimorphism. The degree of dimorphism for traits was significantly negatively associated with the strength of the between-sex correlation. The structure of genetic correlations among life-history traits was more divergent between the two populations in females than in males. Collectively, these results suggest that genetic correlations do not impose a lasting constraint on the evolution of life-history variation in the species.     

Sex ratio represents a unique context for selection on attractive traits: consequences for the evolution of sexual dimorphism

We explored the idea that sex ratio represents a unique context for selection on attractive traits by manipulating sex ratio and pollinator abundance in experimental populations of a gender-dimorphic wild strawberry Fragaria virginiana. We found that increasing the frequency of functional males (the pollen-bearing morph) increased the frequency of pollen-collecting syrphid flies in the pollinator assemblage, decreased pollinator visitation to less preferred morph (females), and decreased the degree of pollen limitation of females. Moreover, sex ratio influenced the strength of selection on petal size through female fitness but did not alter the strength of selection through male fitness components, suggesting that sex ratio can alter the gender bias of selection on an attractive trait. This study of context-dependent selection has important implications for the evolution of sexual dimorphism in attractive traits. First, it suggests that only certain conditions generate male-biased selection and, thus, could lead to selection-driven male-biased petal size dimorphism. Second, it suggests that flexible pollinator foraging may be an important mechanism by which sex ratio influences selection on attractive traits. Finally, it implies that variation in sex ratio could limit the evolution of sexual dimorphism and/or could maintain genetic variation in attractive traits.     

Constraints on the evolution of males and sexual dimorphism: field estimates of genetic architecture of reproductive traits in three populations of gynodioecious Fragaria virginiana

Abstract To understand how genetic constraints may limit the evolution of males and sexual dimorphism in a gynodioecious species, I conducted a quantitative genetic experiment in a gynodioecious wild strawberry, Fragaria virginiana . I estimated and compared genetic parameters (narrow-sense heritabilities, between-trait and between-sex genetic correlations, as well as phenotypic and genetic variance-covariance matrices) in the two sex morphs from three populations grown in a common field garden. I measured pollen and ovule production per flower, petal size, fruit set, and flower number. My major findings are as follows. (1) The presence of a phenotypic trade-off between pollen production and fruit set in hermaphrodites reflects a negative genetic correlation in the narrow sense that is statistically significant when pooled across populations. (2) The main constraints on the evolution of males are low genetic variation for pollen per flower and strong positive correlations associated with ovule number (e.g., between pollen and ovules in hermaphrodites, and between ovules in hermaphrodites and females). (3) Traits with the lowest levels of sexual dimorphism (ovule number and flower number) have the highest between-sex genetic correlations suggesting that overlap in the expression of genes in the sex morphs constrains their independent evolution. (4) There are significant differences in G matrices between sex morphs but not among populations. However, evidence that male-female trait correlations in hermaphrodites were lower in populations with higher frequencies of females may indicate subtle changes in genetic architecture.     

Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates

The goals of this study were to analyze the origin and function of sex differences in the size of canine teeth among Malagasy lemurs and other strepsirhine primates. These analyses allowed me to illuminate interactions between different mechanisms of sexual selection and to elucidate constraints on this sexually-selected trait. In contrast to central predictions of sexual selection theory, polygynous lemurs lack both sexual dimorphism in body size and male social dominance, but the degree of sexual dimorphism in the size of their canines is not known. A comparison of male and female canine size in 31 species of lemurs and lorises revealed significant male-biased canine dimorphism in only 6 of 13 polygynous lemur species. This result is in contrast to predictions of a hypothesis that would explain the lack of size dimorphism in lemurs as a result of high viability costs because canine teeth presumably have low maintenance costs and because they are used as weapons in male-male combat. Moreover, because females had significantly larger maxillary canines than males in only one lemur species, female dominance is not generally based on female physical superiority and selective forces favoring female dominance do not constrain sexual canine dimorphism in the sense of a pleiotropic effect. Contrary to predictions of sexual selection theory, species differences in canine dimorphism across strepsirhines were neither associated with differences in mating system, nor with the potential frequency of aggression. Variation in canine dimorphism was also unrelated to differences in body size, but there were significant differences among families, pointing to strong phylogenetic constraints. This study demonstrated that polygynous lemurs are at most subject to weak intrasexual selection on dental traits used in male combat and that traits thought to be under intense sexual selection are strongly influenced by phylogenetic factors.     

A MULTIVARIATE ANALYSIS OF GENETIC VARIATION IN THE ADVERTISEMENT CALL OF THE GRAY TREEFROG,HYLA VERSICOLOR

Genetic variation in sexual displays is crucial for an evolutionary response to sexual selection, but can be eroded by strong selection. Identifying the magnitude and sources of additive genetic variance underlying sexually selected traits is thus an important issue in evolutionary biology. We conducted a quantitative genetics experiment with gray treefrogs (Hyla versicolor) to investigate genetic variances and covariances among features of the male advertisement call. Two energetically expensive traits showed significant genetic variation: call duration, expressed as number of pulses per call, and call rate, represented by its inverse, call period. These two properties also showed significant genetic covariance, consistent with an energetic constraint to call production. Combining the genetic variance–covariance matrix with previous estimates of directional sexual selection imposed by female preferences predicts a limited increase in call duration but no change in call rate despite significant selection on both traits. In addition to constraints imposed by the genetic covariance structure, an evolutionary response to sexual selection may also be limited by high energetic costs of long‐duration calls and by preferences that act most strongly against very short‐duration calls. Meanwhile, the persistence of these preferences could be explained by costs of mating with males with especially unattractive calls.     

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.     

The evolution of condition-dependent sexual dimorphism

Theory suggests that the net benefit of allocating resources to a sexual trait depends both on the strength of sexual selection on that trait and on individual condition. This predicts a tight coevolution between sexual dimorphism and condition dependence and suggests that these patterns of within-sex and between-sex variation may share a common genetic and developmental basis. Although condition-dependent expression of sexual traits is widely documented, the extent of covariation between condition dependence and sexual dimorphism remains poorly known. I investigated the effects of condition (larval diet quality) on multivariate sexual dimorphism in the fly Telostylinus angusticollis (Neriidae). Condition determined the direction of sexual size dimorphism and modulated sexual shape dimorphism by affecting allometric slopes and/or intercepts of sexually homologous traits in both sexes. Although the greatest responses to condition manipulation were observed in male sexual traits, both sexual and nonsexual traits exhibited substantial variation in the nature and magnitude of condition effects. Nonetheless, condition dependence and sexual dimorphism were remarkably congruent: variation in the strength of condition effects on male traits explained more than 90% of the variation in the magnitude of sexual dimorphism, whether quantified in terms of trait size or allometric slope. The genetic mechanisms that give rise to multivariate sexual dimorphism in body shape thus function in a strongly condition-dependent manner in this species, suggesting a common genetic basis for body shape variation within and between sexes.     

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.