Among‐population variation and correlations in sexually dimorphic traits of Silene latifolia

Abstract The degree of sexual dimorphism in a trait may be determined directly by disruptive selection, as well as by correlations with other traits under selection. We grew seeds from nine populations of the dioecious plant Silene latifolia in a common‐garden experiment to determine whether phenotypic variation and correlations existed for floral, leaf and resource allocation traits, and whether this variation had a genetic component. We also determined the traits which were sexually dimorphic, the degree of dimorphism, and whether it varied among populations. Seven traits exhibited among‐population variation and sexual dimorphism. Variation in the degree of dimorphism occurred only for two traits, suggesting that dimorphism may be evolving more slowly than trait means. Males had more, smaller flowers, shorter leaves, and allocated less of their total biomass to stems and more to leaves than females. Flower production was the most sexually dimorphic trait and was correlated with all measured traits. Most traits exhibited significant correlations between the sexes. The pattern of correlations and the degree of sexual dimorphism among traits lead us to suggest that intrasexual selection for an exaggerated floral display in males has indirectly led to sexual dimorphism in a host of other traits.     

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.     

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.     

THE QUANTITATIVE GENETICS OF SEXUAL DIMORPHISM IN SILENE LATIFOLIA (CARYOPHYLLACEAE). II. RESPONSE TO SEX-SPECIFIC SELECTION

A well-established theoretical relationship exists between genetic correlations between the sexes and the dynamics of response to sex-specific selection. The present study investigates the response to sex-specific selection for two sexually dimorphic traits that have been documented to be genetically variable, calyx diameter and flower number, in Silene latifolia. Following the establishment of a base generation with a known genetic background, selection lines were established and two generations of sex-specific selection were imposed. Calyx diameter responded directly to sex-specific selection, and the positive genetic correlation between the sexes was reflected in correlated responses in the sex that was not the basis for selection within a particular line. Flower number showed a more erratic response to sex-specific selection in that selection in some lines was initially in the wrong direction, that is, selection for a decrease in flower number resulted in an increase. These erratic responses were attributable to genotype-environment interaction as reflected in significant heteroscedasticity in variance among families. Correlated responses to selection in the sex that was not the immediate basis for selection indicated the possible existence of a negative genetic correlation between the sexes for this trait. These results test for the first time the impact of genetic correlations between the sexes on the evolutionary dynamics of sexually dimorphic traits in a plant species.     

Sexually dimorphic inflorescence traits in a wind-pollinated species: heritabilities and genetic correlations in Schiedea adamantis (Caryophyllaceae)

Sexual dimorphism may be especially pronounced in wind-pollinated species because they lack the constraints of biotically pollinated species that must present their pollen and stigmas in similar positions to ensure pollen transfer. Lacking these constraints, the sexes of wind-pollinated species may diverge in response to the different demands of pollen dispersal and receipt, depending on the magnitude of genetic correlations preventing divergence between sexes. Patterns of sexual dimorphism and genetic variation were investigated for inflorescence traits in Schiedea adamantis (Caryophyllaceae), a species well adapted to wind-pollination, and compared to S. salicaria, a species with fewer adaptations to wind pollination. For S. adamantis, dimorphism was pronounced for inflorescence condensation and its components, including lateral flower number and pedicel length. Within sexes, genetic correlations between traits may constrain the relative shape of the inflorescence. Correlations detected across sexes may retard the evolution of sexual dimorphism in inflorescence structure, including features favoring enhanced dispersal and receipt of pollen. Despite genetic correlations across sexes, common principal components analysis showed that genetic variance-covariance matrices (G matrices) differed significantly between the sexes, in part because of greater genetic variation for flower number in hermaphrodites than in females. G matrices also differed between closely related S. adamantis and S. salicaria, indicating the potential for divergent evolution of inflorescence structure despite general similarities in morphology and pollination biology.     

Genetic constraints on floral evolution in a sexually dimorphic plant revealed by artificial selection

Sexual dimorphism is one of the most widespread and recognizable patterns of phenotypic variation in the biotic world. Sexual dimorphism in floral display is striking in the dioecious plant Silene latifolia, with males making many, small flowers compared to females. We investigated this dimorphism via artificial selection on two populations to determine whether genetic variation exists within populations for flower size and the extent of the between-sex correlation, whether a flower size and number trade-off exists within each sex, and whether pollen and ovule production vary with flower size. We selected for decreased flower size (calyx width) in females and increased flower size in males and measured the response to selection in size and correlated responses in flower dry mass, flower number, and pollen or ovule number per flower. Four bouts of selection in each of two selection programs were performed, for a total of three selection lines to decrease size, three to increase it, and two control lines. Flower size always significantly responded to selection and we always found a significant correlated response in the sex not under selection. Selection decreased but did not eliminate the sexual dimorphism in flower dry mass and number. A negative relationship between flower size and number within each sex was revealed. Whereas ovule number showed a significant correlated response to selection on flower size, pollen number did not. Our results indicate that although substantial additive genetic variation for flower size exists, the high between-sex genetic correlation would likely constrain flower size from becoming more sexually dimorphic. Furthermore, floral display within each sex is constrained by a flower size and number trade-off. Given this trade-off and lack of variation in pollen production with flower size, we suggest that sexual dimorphism evolved via sexual selection to increase flower number in males but not females.     

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 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.     

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 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.     

Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size

Models of sexual selection in a cline predict the patterns of clinal variation in female mate preference and male secondary sexual characters. These predictions were tested for the nominate subspecies of the barn swallow Hirundo rustica which demonstrates clinal variation in morphology, with several characters in both sexes showing increasing size at higher latitudes. Sexual size dimorphism in the length of the tail ornament and the short, central tail feathers increase with increasing latitude while size dimorphism in other morphological characters is independent of latitude. The main reason for the two divergent patterns of sexual size dimorphism appears to be the higher foraging cost of having a long tail ornamental at low latitudes. The control of development decreases with increasing latitude as demonstrated by an increasing latitudinal cline in fluctuating asymmetry of tail length. Phenotypic variance in tail length increases with latitude in males, but not in females, as shown by the coefficients of variation. Clinal variation in morphology is not due to natural selection associated with a latitudinal increase in the distance between breeding and wintering areas. The geographic patterns of morphological variation suggest that the tail character has diverged geographically as a result of a sexual process of reliable signalling.     

Dioecious Silene at the X-road: the reasons Y

Among the variety of breeding systems developed by flowering plants, those based on heteromorphic sex chromosomes are the most intellectually challenging in evolutionary terms. This is because, among other things, they enable us to compare sex determination processes between plants and animals. White campion (Silene latifolia, also named Lychnis or Melandrium) is dioecious and, much like us, females are homogametic (XX) and males are heterogametic (XY). Sexual dimorphism in white campion is controlled by two independent developmental pathways operating from the Y chromosome at very early developmental stages and within distinct regions of the flower. In addition, all basic steps in the evolution from the bisexual to the dioecious condition with heteromorphic sex chromosomes are known and available to experimentation in the genus Silene. This group of species has been under scrutiny for more than a century. Such an ideal experimental system enables us to tackle, with novel methodological tools, several classical questions in biology. These include the question of how sexual dimorphism evolved and how dimorphic development is controlled, as well as questions of how sex chromosomes evolve in the absence of meiotic recombination or how male-female genetic conflicts are generated. At the turn of the century, the time is now ripe to have a closer look. Received: 21 September 1999 / Accepted: 11 October 1999     

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 variation for sexual dimorphism in flower size within and between populations of gynodioecious Thymus vulgaris

There has been very little empirical study of quantitative genetic variation in flower size in sexually dimorphic plant species, despite the frequent occurrence of flower size differences between sexual phenotypes. In this study we quantify the nature of quantitative flower size variation in females and hermaphrodites of gynodioecious Thymus vulgaris. In a field study, females had significantly smaller flowers than hermaphrodites, and the degree of flower size dimorphism varied significantly among populations. To quantify the genetic basis of flower size variation we sampled maternal progeny from 10 F₀ females in three populations (across the range of variation in flower size in the field), performed controlled crosses on F₁ offspring in the glasshouse and grew F₂ progeny to flowering in uniform field conditions. A significant population * sex interaction was again observed, hence the degree of sexual dimorphism shows genetic variation among populations. A significant family * sex interaction was also observed, indicating that the degree of sexual dimorphism shows genetic variation among families. Females showed significantly greater variation among populations and among families than hermaphrodites. Female flower size varied significantly depending on the degree of stamen abortion, with morphologically intermediate females having flowers more similar to hermaphrodites than to other females. The frequency of female types that differ in the degree of stamen abortion varied among populations and families and mean family female flower size increased as the proportion of intermediate female types increased across families. Variation in the degree of flower size dimorphism thus appears to be a result of variation in the degree of stamen abortion in females, the potential causes of which are discussed.     

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.     

Correlated responses to selection on female egg size in male reproductive traits in a butterfly

Genetic correlations between male and female traits can act as evolutionary constraints and, if involving reproductive traits, potentially influence sexual selection. Artificial selection on egg size in the tropical butterfly Bicyclus anynana has yielded highly divergent lines. Here we report evidence for correlated evolution in male traits. Males from the large-egg selected lines produced significantly heavier spermatophores independent of body size and tended to have more fertile sperm stored in their reproductive tracts than those from the small-egg selected lines. This may be due to an underlying genetic correlation in reproductive effort between the sexes. However, non-fertile sperm number and testis size remained unaffected by selection on egg size. Phenotypic correlations within an unselected population revealed that spermatophore mass and fertile sperm number, but not testis size and non-fertile sperm number, were positively related to male body size, and that larger spermatophores contained more fertile, but not non-fertile sperm. In addition, males provided larger females with bigger spermatophores and more fertile sperm, indicating males may be exercising mate choice during copulation.     

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 QUANTITATIVE GENETICS AND COEVOLUTION OF MALE AND FEMALE REPRODUCTIVE TRAITS

Studies of experimental sexual selection have tested the effect of variation in the intensity of sexual selection on male investment in reproduction, particularly sperm. However, in several species, including Drosophila pseudoobscura, no sperm response to experimental evolution has occurred. Here, we take a quantitative genetics approach to examine whether genetic constraints explain the limited evolutionary response. We quantified direct and indirect genetic variation, and genetic correlations within and between the sexes, in experimental populations of D. pseudoobscura. We found that sperm number may be limited by low heritability and evolvability whereas sperm quality (length) has moderate V_A and CV_A but does not evolve. Likewise, the female reproductive tract, suggested to drive the evolution of sperm, did not respond to experimental sexual selection even though there was sufficient genetic variation. The lack of genetic correlations between the sexes supports the opportunity for sexual conflict over investment in sperm by males and their storage by females. Our results suggest no absolute constraint arising from a lack of direct or indirect genetic variation or patterns of genetic covariation. These patterns show why responses to experimental evolution are hard to predict, and why research on genetic variation underlying interacting reproductive traits is needed.     

Subtle,pervasive genetic correlation between the sexes in the evolution of dimorphic hummingbird tail ornaments*

Male hummingbirds have repeatedly evolved sexually dimorphic tails that they use as ornaments during courtship. We examine how male ornament evolution is reflected in female morphology. Lande's two-step model of the evolution of dimorphism predicts that γ (the genetic correlation between the sexes) causes trait elaboration to first evolve quickly in both sexes, then dimorphism evolves more slowly. On the hummingbird phylogeny, tail length does not fit this two-step model; although hummingbirds repeatedly evolved ornamental, elongated tails, dimorphism evolves on the same phylogenetic branch as elongation, implying that γ quickly evolves to be low over phylogenetic timescales. Male “bee” hummingbirds have evolved diverse rectrix shapes that they use to produce sound. Female morphologies exhibit subtle, pervasive correlations with male morphology. No female-adaptive hypotheses explain these correlations, since females do not also make sounds with their tail. Subtle shape similarity has arisen through the genetic correlation with males, and is subject to intralocus sexual conflict. Intralocus sexual conflict may produce increased phenotypic variation of female ornaments. Other evolutionary constraints on tail morphology include a developmental correlation between neighboring tail-feathers, biasing tail elaboration to occur most often at the ends of the feather tract (rectrix 5 or 1) and not the middle.