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.     

Indirect evidence from DNA sequence diversity for genetic degeneration of the Y-chromosome in dioecious species of the plant Silene: the SlY4/SlX4 and DD44-X/DD44-Y gene pairs

The action of natural selection is expected to reduce the effective population size of a nonrecombining chromosome, and this is thought to be the chief factor leading to genetic degeneration of Y-chromosomes, which cease recombining during their evolution from ordinary chromosomes. Low effective population size of Y chromosomes can be tested by studying DNA sequence diversity of Y-linked genes. In the dioecious plant, Silene latifolia, which has sex chromosomes, one comparison (SlX1 vs. SlY1) indeed finds lower Y diversity compared with the homologous X-linked gene, and one Y-linked gene with no X-linked homologue has lower species-wide diversity than a homologous autosomal copy (SlAp3Y vs. SlAp3A). To test whether this is a general pattern for Y-linked genes, we studied two further recently described X and Y homologous gene pairs in samples from several populations of S. latifolia and S. dioica. Diversity is reduced for both Y-linked genes, compared with their X-linked homologues. Our new data are analysed to show that the low Y effective size cannot be explained by different levels of gene flow for the X vs. the Y chromosomes, either between populations or between these closely related species. Thus, all four Y-linked genes that have now been studied in these plants (the two studied here, and two previously studied genes, have low diversity). This supports other evidence for an ongoing degeneration process in these species.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Analysis of the G-overhang structures on plant telomeres: evidence for two distinct telomere architectures

Telomeres are highly conserved structures essential for maintaining the integrity of eukaryotic genomes. In yeast, ciliates and mammals, the G-rich strand of the telomere forms a 3' overhang on the chromosome terminus. Here we investigate the architecture of telomeres in the dicot plants Silene latifolia and Arabidopsis thaliana using the PENT (primer extension/nick translation) assay. We show that both Arabidopsis and Silene telomeres carry G-overhangs longer than 20-30 nucleotides. However, in contrast to yeast and ciliate telomeres, only half of the telomeres in Silene seedlings possess detectable G-overhangs. PENT reactions using a variety of primers and reaction conditions revealed that the remaining fraction of Silene telomeres carries either no overhangs or overhangs less than 12 nucleotides in length. G-overhangs were observed in Silene seeds and leaves, tissues that lack telomerase activity. These findings suggest that incomplete DNA replication of the lagging strand, rather than synthesis by telomerase, is the primary mechanism for G-overhang synthesis in plants. Unexpectedly, we found that the fraction of telomeres with detectable G-overhangs decreased from 50% in seedlings to 35% in leaves. The difference may reflect increased susceptibility of the G-overhangs to nuclease attack in adult leaves, an event that could act as a precursor for the catabolic processes accompanying leaf senescence     

Experimental evidence for accelerated adaptation to desiccation through sexual selection on males

The impact of sexual selection on the adaptive process remains unclear. On the one hand, sexual selection might hinder adaptation by favouring costly traits and preferences that reduce nonsexual fitness. On the other hand, condition dependence of success in sexual selection may accelerate adaptation. Here, we used replicate populations of Drosophila melanogaster to artificially select on male desiccation resistance while manipulating the opportunity for precopulatory sexual selection in a factorial design. Following five generations of artificial selection, we measured the desiccation resistance of males and females to test whether the addition of sexual selection accelerated adaptation. We found a significant interaction between the effects of natural selection and sexual selection: desiccation resistance was highest in populations where sexual selection was allowed to operate. Despite only selecting on males, we also found a correlated response in females. These results provide empirical support for the idea that sexual selection can accelerate the rate of adaptation.     

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.     

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.     

Sexual, fecundity, and viability selection on flower size and number in a sexually dimorphic plant

The evolution of sexual dimorphism will depend on how sexual, fecundity and viability selection act within each sex, with the different forms of selection potentially operating in opposing directions. We examined selection in the dioecious plant Silene latifolia using planted arrays of selection lines that differed in flower size (small vs. large). In this species, a flower size/number trade-off exists within each sex, and males produce smaller and more numerous flowers than females. Moreover, floral traits are genetically correlated with leaf physiology. Sexual selection favoring males in the small-flower line occurred via greater overlap in the timing of flower output between males from this line and females. Fecundity selection favored males with high flower production, as siring success was proportionate to pollen production. Viability selection opposed sexual selection, favoring males from the large-flower line. In females, fecundity and viability selection operated in the same direction, favoring those from the large-flower line via greater seed production and survival. These results concur with the pattern of floral sexual dimorphism. Together with previous results they suggest that the outcome of the different forms of selection will be environmentally dependent, and therefore help to explain variation among populations in sexually dimorphic traits.     

Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection

With a small effective population size, random genetic drift is more important than selection in determining the fate of new alleles. Small populations therefore accumulate deleterious mutations. Left unchecked, the effect of these fixed alleles is to reduce the reproductive capacity of a species, eventually to the point of extinction. New beneficial mutations, if fixed by selection, can restore some of this lost fitness. This paper derives the overall change in fitness due to fixation of new deleterious and beneficial alleles, as a function of the distribution of effects of new mutations and the effective population size. There is a critical effective size below which a population will on average decline in fitness, but above which beneficial mutations allow the population to persist. With reasonable estimates of the relevant parameters, this critical effective size is likely to be a few hundred. Furthermore, sexual selection can act to reduce the fixation probability of deleterious new mutations and increase the probability of fixing new beneficial mutations. Sexual selection can therefore reduce the risk of extinction of small populations.     

Comparison of t-tests for differences in sexual dimorphism between populations

A t-test that can be used for evaluating the significance of differences in metric sexual dimorphism between populations is derived directly from mathematical considerations of the differences between distributions. It is compared with the t-test derived by Relethford and Hodges (1985), which was based upon linear regression with sex as a dummy variable. Both are determined to be mathematically equivalent, though the one derived here is more similar in form to traditional t-tests of differences and therefore may be simpler to employ. Both tests require only summary statistics for comparisons between populations and comparisons between generations within populations.     

Sexual selection without sexual dimorphism: Bateman gradients in a simultaneous hermaphrodite

One of the most general patterns in sexual selection is stronger selection on mating activity in males than in females. This asymmetry is thought to result from the higher energetic cost of producing one female compared to one male gamete (anisogamy). However, most studies focused on gonochoric species with strong sexual dimorphism, in which males and females are necessarily under different selection regimes. The question remains whether anisogamy alone would suffice to produce such differences. In simultaneous hermaphrodites one can compare sexual selection on the male and female functions in the absence of sexual dimorphism. Here we quantify sexual selection in the hermaphroditic freshwater snail Physa acuta under laboratory conditions. We combine exhaustive behavioral records of mating activity in mating groups and molecular paternity assignment to measure the mating success and reproductive success of 120 individuals. Our results validate the prediction of stronger selection to gain mating partners in the male than in the female function. Moreover, we did not detect cross‐sex effects on fitness, or correlations between male and female production of offspring over the course of our experiment. We conclude that with respect to sexual selection P. acuta is comparable to gonochorists, confirming that anisogamy is a sufficient explanation for the differences in sexual selection regimes between sexes.     

A statistical test for differences in sexual dimorphism between populations

Many studies involve comparison of measures of sexual dimorphism between two samples. This comparison is used to test a variety of hypotheses, such as changing environmental conditions. Methods for testing the significance of the difference between two populations tend to be complex, and/or require access to complete original data. We offer a simplified approach which is based on a linear regression model using dummy variables. Our method is computationally simple and can be used with summary statistics (sample size, means, standard deviations) instead of raw data. We present three examples of the application of our method to problems in physical anthropology. We also note that our method has a broader range of applications apart from that of sexual dimorphism.     

Dynamics of drift, gene flow, and selection during speciation in Silene

The mechanics of speciation with gene flow are still unclear. Disparity among genes in population differentiation (F(ST)) between diverging species is often interpreted as evidence for semipermeable species boundaries, with selection preventing "key" genes from introgressing despite ongoing gene flow. However, F(ST) can remain high before it reaches equilibrium between the lineage sorting of species divergence and the homogenizing effects of gene flow (via secondary contact). Thus, when interpreting F(ST), the dynamics of drift, gene flow, and selection need to be taken into account. We illustrate this view with a multigenic analyses of gene flow and selection in three closely related Silene species, S. latifolia, S. dioica, and S. diclinis. We report that although S. diclinis appears to have evolved in allopatry, isolation with (bidirectional) gene flow between S. latifolia and S. dioica is likely, perhaps as a result of parapatric speciation followed by more extensive sympatry. Interestingly, we detected the signatures of apparently independent instances of positive selection at the same locus in S. latifolia and S. dioica. Despite gene flow between the species, the adaptive alleles have not crossed the species boundary, suggesting that this gene has independently undergone species-specific (diversifying or parallel) selection.     

The consequences of sexual selection in well‐adapted and maladapted populations of bean beetles†

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex‐specific strengths of selection and IaSC by cross‐rearing the two experimental evolution regimes on the alternative hosts and estimating within‐population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male‐bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.     

Sexual dimorphism in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

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.     

Scale dependence of sex ratio in wild plant populations: implications for social selection

Social context refers to the composition of an individual''s social interactants, including potential mates. In spatially structured populations, social context can vary among individuals within populations, generating the opportunity for social selection to drive differences in fitness functions among individuals at a fine spatial scale. In sexually polymorphic plants, the local sex ratio varies at a fine scale and thus has the potential to generate this opportunity. We measured the spatial distribution of two wild populations of the gynodioecious plant Silene vulgaris and show that there is fine‐scale heterogeneity in the local distribution of the sexes within these populations. We demonstrate that the largest variance in sex ratio is among nearest neighbors. This variance is greatly reduced as the spatial scale of social interactions increases. These patterns suggest the sex of neighbors has the potential to generate fine‐scale differences in selection differentials among individuals. One of the most important determinants of social interactions in plants is the behavior of pollinators. These results suggest that the potential for selection arising from sex ratio will be greatest when pollen is shared among nearest neighbors. Future studies incorporating the movement of pollinators may reveal whether and how this fine‐scale variance in sex ratio affects the fitness of individuals in these populations.     

Adaptive divergence for a fitness-related trait among invasive Ambrosia artemisiifolia populations in France

The impact of natural selection on the adaptive divergence of invasive populations can be assessed by testing the null hypothesis that the extent of quantitative genetic differentiation (Q(ST) ) would be similar to that of neutral molecular differentiation (F(ST) ). Using eight microsatellite loci and a common garden approach, we compared Q(ST) and F(ST) among ten populations of an invasive species Ambrosia artemisiifolia (common ragweed) in France. In a common garden study with varying water and nutrient levels, we measured Q(ST) for five traits (height, total biomass, reproductive allocation, above- to belowground biomass ratio, and days to flowering). Although low F(ST) indicated weak genetic structure and strong gene flow among populations, we found significant diversifying selection (Q(ST) > F(ST) ) for reproductive allocation that may be closely related to fitness. It suggests that abiotic conditions may have exerted selection pressure on A. artemisiifolia populations to differentiate adaptively, such that populations at higher altitude or latitude evolved greater reproductive allocation. As previous studies indicate multiple introductions from various source populations of A. artemisiifolia in North America, our results suggest that the admixture of introduced populations may have increased genetic diversity and additive genetic variance, and in turn, promoted the rapid evolution and adaptation of this invasive species.     

Cast adrift on an island: introduced populations experience an altered balance between selection and drift

A long-standing question in evolutionary biology is what becomes of adaptive traits when a species expands its range into novel environments. Here, we report the results of a study on an adaptive colour pattern polymorphism (stripes) of the coqui frog, Eleutherodactylus coqui, following its introduction to Hawaii from Puerto Rico. We compared population differentiation ( ) for the stripes locus-which underlies this colour pattern polymorphism-with neutral microsatellite loci to test for a signature of selection among native and introduced populations. Among native populations, for stripes were lower than expected under the neutral model, suggesting uniform balancing selection. Alternatively, among introduced populations, for stripes did not differ from the neutral model. These results suggest that the evolutionary dynamics of this previously adaptive trait have become dominated by random genetic drift following the range expansion.