Sexual selection in females and the evolution of polyandry.

Over the last decades, the field of sexual selection underwent a paradigm shift from sexual-stereotype thinking of "eager" males and "coy" females towards a more nuanced perspective acknowledging that not only males but also females can benefit from multiple mating and compete for mating partners. Yet, sexual selection in females is still considered a peculiarity, and the evolution of polyandry is often viewed to result from a higher mating interest of males. Here, we present meta-analytic evidence from 77 species across a broad range of animal taxa to demonstrate that female reproductive success is overall positively correlated with mating success, suggesting that females typically benefit from multiple mating. Importantly, we found that these fitness gains likely promote the evolution of polyandry. Our findings offer support for the idea that sexual selection is widespread in females and to play a key role for the evolution of animal mating systems. Thereby, our results extend our understanding of the evolutionary consequences of sexual reproduction and contribute to a more balanced view of how sexual selection operates in males and females.

Sperm competition favours intermediate sperm size in a hermaphrodite1.

Sperm competition is a potent mechanism of postcopulatory sexual selection that has been found to shape reproductive morphologies and behaviours in promiscuous animals. Especially sperm size has been argued to evolve in response to sperm competition through its effect on sperm longevity, sperm motility, the ability to displace competing sperm, and ultimately fertilization success. Additionally, sperm size has been observed to co-evolve with female reproductive morphology. Theoretical work predicts that sperm competition may select for longer sperm but may also favour shorter sperm if sperm size trades-off with number. In this study, we studied the relationship between sperm size and postmating success in the free-living flatworm, Macrostomum lignano. Specifically, we used inbred isolines of M. lignano that varied in sperm size to investigate how sperm size translated into the ability of worms to transfer and deposit sperm in a mating partner. Our results revealed a hump-shaped relationship with individuals producing sperm of intermediate size having the highest sperm competitiveness. This finding broadens our understanding of the evolution of sperm morphology by providing empirical support for stabilizing selection on sperm size under sperm competition.

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite.

Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

Sexual selection and sexual size dimorphism in animals.

Sexual selection is often considered as a critical evolutionary force promoting sexual size dimorphism (SSD) in animals. However, empirical evidence for a positive relationship between sexual selection on males and male-biased SSD received mixed support depending on the studied taxonomic group and on the method used to quantify sexual selection. Here, we present a meta-analytic approach accounting for phylogenetic non-independence to test how standardized metrics of the opportunity and strength of pre-copulatory sexual selection relate to SSD across a broad range of animal taxa comprising up to 95 effect sizes from 59 species. We found that SSD based on length measurements was correlated with the sex difference in the opportunity for sexual selection but showed a weak and statistically non-significant relationship with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of SSD in a broad phylogenetic context.

Assortative Mating in Animals and Its Role for Speciation.

Evolutionary theory predicts that positive assortative mating-the tendency of similar individuals to mate with each other-plays a key role for speciation by generating reproductive isolation between diverging populations. However, comprehensive tests for an effect of assortative mating on species richness at the macroevolutionary scale are lacking. We used a meta-analytic approach to test the hypothesis that the strength of assortative mating within populations is positively related to species richness across a broad range of animal taxa. Specifically, we ran a phylogenetically independent meta-analysis using an extensive database of 1,447 effect sizes for the strength of assortative mating, encompassing 307 species from 130 families and 14 classes. Our results suggest that there is no relationship between the strength of assortative mating and species richness across and within major taxonomic groups and trait categories. Moreover, our analysis confirms an earlier finding that animals typically mate assortatively (global Pearson correlation coefficient: r=0.36; 95% confidence interval: 0.19-0.52) when accounting for phylogenetic nonindependence. We argue that future advances will rely on a better understanding of the evolutionary causes and consequences of the observed intra- and interspecific variation in the strength of assortative mating.

Operational sex ratio predicts the opportunity and direction of sexual selection across animals.

The operational sex ratio (OSR) has long been assumed to be a key ecological factor determining the opportunity and direction of sexual selection. However, recent theoretical work has challenged this view, arguing that a biased OSR does not necessarily result in greater monopolisation of mates and therefore stronger sexual selection in the mate-limited sex. Hence, the role of the OSR for shaping animal mating systems remains a conundrum in sexual selection research. Here we took a meta-analytic approach to test whether OSR explains interspecific variation in sexual selection metrics across a broad range of animal taxa. Our results demonstrate that the OSR predicts the opportunity for sexual selection in males and the direction of sexual selection in terms of sex differences in both the opportunity for sexual selection and the Bateman gradient (i.e. the selection differential of mating success), as predicted by classic theory.

Sexual selection predicts species richness across the animal kingdom.

Our improving knowledge of the animal tree of life consistently demonstrates that some taxa diversify more rapidly than others, but what contributes to this variation remains poorly understood. An influential hypothesis proposes that selection arising from competition for mating partners plays a key role in promoting speciation. However, empirical evidence showing a link between proxies of this sexual selection and species richness is equivocal. Here, we collected standardized metrics of sexual selection for a broad range of animal taxa, and found that taxonomic families characterized by stronger sexual selection on males show relatively higher species richness. Thus, our data support the hypothesis that sexual selection elevates species richness. This could occur either by promoting speciation and/or by protecting species against extinction.

Environment-Dependent Sexual Selection: Bateman's Parameters under Varying Levels of Food Availability.

Sexual selection is a potent evolutionary force that has been shown to vary in strength and direction depending on demographic factors such as density and sex ratio. However, the effect of other environmental factors on the mode of sexual selection remains largely unexplored. Here, we tested experimentally how food restriction affects the potential for sexual selection in the male and the female sex function of the simultaneously hermaphroditic freshwater snail Physa acuta. We manipulated food availability and compared Bateman's metrics of sexual selection between groups of five well-fed and five food-restricted snails. Food-restricted individuals had a reduced female reproductive output, suggesting that we successfully manipulated the reproductive resources. Importantly, food restriction reduced the male opportunity for sexual selection (in terms of a lowered variance in male mating success) and led to diminishing returns of mating in both sexes (in terms of nonsignificant Bateman gradients). Furthermore, we observed significant changes in the relative contribution of different fitness components, suggesting stronger postcopulatory selection in the male sex role and stronger fecundity selection in the female sex role under restricted food conditions. This study highlights the need to incorporate ecological factors to better understand how sexual selection operates in the wild.

Fluorescent sperm in a transparent worm: validation of a GFP marker to study sexual selection.

BACKGROUND: Sexual selection has initially been thought to occur exclusively at the precopulatory stage in terms of contests among males and female mate choice, but research over the last four decades revealed that it often continues after copulation through sperm competition and cryptic female choice. However, studying these postcopulatory processes remains challenging because they occur internally and therefore are often difficult to observe. In the transparent free-living flatworm Macrostomum lignano, a recently established transgenic line that expresses green fluorescent protein (GFP) in all cell types, including sperm, offers a unique opportunity to non-invasively visualise and quantify the sperm of a GFP-expressing donor inside the reproductive tract of wild-type recipients in vivo. We here test several aspects of the reproductive performance of the transgenic individuals and the accuracy of the techniques involved in assessing the GFP-expressing worms and their sperm. We then show the usefulness of these methods in a study on sperm displacement. RESULTS: GFP-expressing worms do not differ from wild-type worms in terms of morphology, mating rate and reproductive success. In addition, we show that the GFP signal is reliably and unequivocally expressed by all GFP-expressing individuals observed under epifluorescence illumination. However, the intensity of the GFP signal emitted by sperm of GFP expressing donors can vary (which we show to be at least in part due to sperm ageing) and the GFP marker is inherited according to Mendel's laws in most, but not all, of the individuals. Nevertheless, we argue these two issues can be addressed with an appropriate experimental design. Finally, we demonstrate the value of the GFP-techniques by comparing the number of GFP-expressing sperm in a wild-type recipient before and after mating with a competing sperm donor, providing clear experimental evidence for sperm displacement in M. lignano. This result suggests that sperm donors can displace previously stored sperm and replace it with their own. CONCLUSION: The availability of the GFP-techniques in a transparent organism provide unique opportunities to visualise and quantify internal processes in the female reproductive tract after mating, which opens new avenues in the study of sexual selection.

No fitness effects of same-sex copulations in male red flour beetles.

Same-sex sexual behavior occurs in diverse animal taxa, yet its evolutionary maintenance is poorly understood as such behavior seems to be costly and does not directly increase reproductive success. We used male Tribolium castaneum beetles, which frequently engage in same-sex copulations, to test if same-sex sexual behavior influences future male mating behavior and reproductive success of males. Furthermore, we tested whether same-sex sexual behavior has benefits via indirect sperm translocation. We conducted a series of mating trials demonstrating that males exposed to same-sex behavior did not sire less offspring compared to control males that did not engage in same-sex behavior. This suggests that same-sex copulations did not lead to fitness costs in subsequent mating interactions. In addition, we found no evidence that indirect sperm translocation via an intermediate male occurs in T. castaneum. Taken together, these results imply that same-sex sexual behavior in males is associated with no costs in terms of lower mating rate and reduced siring success and does not seem to entail benefits. Moreover, our data conform to the hypothesis that sexual indiscrimination is prevalent in this species, which may explain the relatively high frequency of same-sex sexual behavior in T. castaneum.

Local adaptation of sex induction in a facultative sexual crustacean: insights from QTL mapping and natural populations of Daphnia magna.

Dormancy is a common adaptation in invertebrates to survive harsh conditions. Triggered by environmental cues, populations produce resting eggs that allow them to survive temporally unsuitable conditions. Daphnia magna is a crustacean that reproduces by cyclical parthenogenesis, alternating between the production of asexual offspring and the sexual reproduction of diapausing eggs (ephippia). Prior to ephippia production, males (necessary to ensure ephippia fertilization) are produced parthenogenetically. Both the production of ephippia and the parthenogenetic production of males are induced by environmental factors. Here, we test the hypothesis that the induction of D. magna resting egg production shows a signature of local adaptation. We postulated that Daphnia from permanent ponds would produce fewer ephippia and males than Daphnia from intermittent ponds and that the frequency and season of habitat deterioration would correlate with the timing and amount of male and ephippia production. To test this, we quantified the production of males and ephippia in clonal D. magna populations in several different controlled environments. We found that the production of both ephippia and males varies strongly among populations in a way that suggests local adaptation. By performing quantitative trait locus mapping with parent clones from contrasting pond environments, we identified nonoverlapping genomic regions associated with male and ephippia production. As the traits are influenced by two different genomic regions, and both are necessary for successful resting egg production, we suggest that the genes for their induction co-evolve.

Evidence for stronger sexual selection in males than in females using an adapted method of Bateman's classic study of Drosophila melanogaster.

Bateman's principles, originally a test of Darwin's theoretical ideas, have since become fundamental to sexual selection theory and vital to contextualizing the role of anisogamy in sex differences of precopulatory sexual selection. Despite this, Bateman's principles have received substantial criticism, and researchers have highlighted both statistical and methodological errors, suggesting that Bateman's original experiment contains too much sampling bias for there to be any evidence of sexual selection. This study uses Bateman's original method as a template, accounting for two fundamental flaws in his original experiments, (a) viability effects and (b) a lack of mating behavior observation. Experimental populations of Drosophila melanogaster consisted of wild-type focal individuals and nonfocal individuals established by backcrossing the brown eye (bw-) eye-color marker-thereby avoiding viability effects. Mating assays included direct observation of mating behavior and total number of offspring, to obtain measures of mating success, reproductive success, and standardized variance measures based on Bateman's principles. The results provide observational support for Bateman's principles, particularly that (a) males had significantly more variation in number of mates compared with females and (b) males had significantly more individual variation in total number of offspring. We also find a significantly steeper Bateman gradient for males compared to females, suggesting that sexual selection is operating more intensely in males. However, female remating was limited, providing the opportunity for future study to further explore female reproductive success in correlation with higher levels of remating.

Diet quality impairs male and female reproductive performance and affects the opportunity for selection in an insect model.

Environmental factors can have profound effects on the strength and direction of selection and recent studies suggest that such environment-dependent selection can be sex-specific. Sexual selection theory predicts that male fitness is more condition dependent compared to female fitness, suggesting that male fitness is more sensitive to environmental stress. However, our knowledge about the effect of environmental factors on sex-specific reproductive performance and on sex differences in the opportunity for selection is still very limited. In the present study, we investigated the sex-specific effects of diet quality (yeast deprivation and flour type) in the red flour beetle Tribolium castaneum. Specifically, we manipulated yeast supplementation in wheat and whole-wheat flour in competition assays allowing us to test for sex-specific effects of food quality (i) on reproductive success and (ii) on the opportunity for selection. Our data show that yeast deprivation in wheat flour had significantly negative effects on body mass and reproductive success of both sexes, while high-quality flour (whole-wheat flour) was able to buffer the negative impact to a large extent. Importantly, our data suggest no sex-specific effect of dietary stress on reproductive success because the magnitude of the negative effect of yeast deprivation was similar for males and females. Moreover, our study demonstrates that low food quality inflated the opportunity for selection and did not differ between sexes neither under benign nor stressful dietary conditions. We discuss the implications of our findings for the adaptation to stressful environments.

Sexual selection moderates heat stress response in males and females.

A widespread effect of climate change is the displacement of organisms from their thermal optima. The associated thermal stress imposed by climate change has been argued to have a particularly strong impact on male reproduction but evidence for this postulated sex-specific stress response is equivocal.One important factor that may explain intra- and interspecific variation in stress responses is sexual selection, which is predicted to magnify negative effects of stress. Nevertheless, empirical studies exploring the interplay of sexual selection and heat stress are still scarce.We tested experimentally for an interaction between sexual selection and thermal stress in the red flour beetle Tribolium castaneum by contrasting heat responses in male and female reproductive success between enforced monogamy and polygamy.We found that polygamy magnifies detrimental effects of heat stress in males but relaxes the observed negative effects in females. Our results suggest that sexual selection can reverse sex differences in thermal sensitivity, and may therefore alter sex-specific selection on alleles associated with heat tolerance.Assuming that sexual selection and natural selection are aligned to favour the same genetic variants under environmental stress, our findings support the idea that sexual selection on males may promote the adaptation to current global warming. Read the free Plain Language Summary for this article on the Journal blog.

Systematic review reveals multiple sexually antagonistic polymorphisms affecting human disease and complex traits.

An evolutionary model for sex differences in disease risk posits that alleles conferring higher risk in one sex may be protective in the other. These sexually antagonistic (SA) alleles are predicted to be maintained at frequencies higher than expected under purifying selection against unconditionally deleterious alleles, but there are apparently no examples in humans. Discipline-specific terminology, rather than a genuine lack of such alleles, could explain this disparity. We undertook a two-stage review of evidence for SA polymorphisms in humans using search terms from (i) evolutionary biology and (ii) biomedicine. Although the first stage returned no eligible studies, the second revealed 51 genes with sex-opposite effects; 22 increased disease risk or severity in one sex but protected the other. Those with net positive effects occurred at higher frequencies. None were referred to as SA. Our review reveals significant communication barriers to fields as a result of discipline-specific terminology.

Stronger net selection on males across animals.

Sexual selection is considered the major driver for the evolution of sex differences. However, the eco-evolutionary dynamics of sexual selection and their role for a population's adaptive potential to respond to environmental change have only recently been explored. Theory predicts that sexual selection promotes adaptation at a low demographic cost only if sexual selection is aligned with natural selection and if net selection is stronger on males compared to females. We used a comparative approach to show that net selection is indeed stronger in males and provide preliminary support that this sex bias is associated with sexual selection. Given that both sexes share the vast majority of their genes, our findings corroborate the notion that the genome is often confronted with a more stressful environment when expressed in males. Collectively, our study supports one of the long-standing key assumptions required for sexual selection to bolster adaptation, and sexual selection may therefore enable some species to track environmental change more efficiently.

The Scope for Postmating Sexual Selection in Plants.

Sexual selection is known to shape plant traits that affect access to mates during the pollination phase, but it is less well understood to what extent it affects traits relevant to interactions between pollen and pistils after pollination. This is surprising, because both of the two key modes of sexual selection, male-male competition and female choice, could plausibly operate during pollen-pistil interactions where physical male-female contact occurs. Here, we consider how the key processes of sexual selection might affect traits involved in pollen-pistil interactions, including 'Fisherian runaway' and 'good-genes' models. We review aspects of the molecular and cellular biology of pollen-pistil interactions on which sexual selection could act and point to research that is needed to investigate them.

Sex allocation predicts mating rate in a simultaneous hermaphrodite.

Sexual selection theory for separate-sexed animals predicts that the sexes differ in the benefit they can obtain from multiple mating. Conventional sex roles assume that the relationship between the number of mates and the fitness of an individual is steeper in males compared with females. Under these conditions, males are expected to be more eager to mate, whereas females are expected to be choosier. Here we hypothesize that the sex allocation, i.e. the reproductive investment devoted to the male versus female function, can be an important predictor of the mating strategy in simultaneous hermaphrodites. We argue that within-species variation in sex allocation can cause differences in the proportional fitness gain derived through each sex function. Individuals should therefore adjust their mating strategy in a way that is more beneficial to the sex function that is relatively more pronounced. To test this, we experimentally manipulated the sex allocation in a simultaneously hermaphroditic flatworm and investigated whether this affects the mating behaviour. The results demonstrate that individuals with a more male-biased sex allocation (i.e. relatively large testes and small ovaries) are more eager to mate compared with individuals with a more female-biased sex allocation (i.e. relatively small testes and large ovaries). We argue that this pattern is comparable to conventional gender roles in separate-sexed organisms.

Sex allocation and sexual conflict in simultaneously hermaphroditic animals.

Links between sex allocation (SA) and sexual conflict in simultaneous hermaphrodites have been evident since Charnov's landmark paper published 30 years ago. We discuss two links, namely the potential for sexual conflict over SA between sperm donor and recipient, and the importance of post-copulatory sexual selection and the resulting sexual conflict for the evolution of SA. We cover the little empirical and theoretical work exploring these links, and present an experimental test of one theoretical prediction. The link between SA and sexual conflict is an interesting field for future empirical and theoretical research.

Asymmetric evolutionary responses to sex-specific selection in a hermaphrodite.

Sex allocation theory predicts that simultaneous hermaphrodites evolve to an evolutionary stable resource allocation, whereby any increase in investment to male reproduction leads to a disproportionate cost on female reproduction and vice versa. However, empirical evidence for sexual trade-offs in hermaphroditic animals is still limited. Here, we tested how male and female reproductive traits evolved under conditions of reduced selection on either male or female reproduction for 40 generations in a hermaphroditic snail. This selection favors a reinvestment of resources from the sex function under relaxed selection toward the other function. We found no such evolutionary response. Instead, juvenile survival and male reproductive success significantly decreased in lines where selection on the male function (i.e., sexual selection) was relaxed, while relaxing selection on the female function had no effect. Our results suggest that most polymorphisms under selection in these lines were not sex-antagonistic. Rather, they were deleterious mutations affecting juvenile survival (thus reducing both male and female fitness) with strong pleiotropic effects on male success in a sexual selection context. These mutations accumulated when sexual selection was relaxed, which supports the idea that sexual selection in hermaphrodites contributes to purge the mutation load from the genome as in separate-sex organisms.