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.

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 102 effect sizes from 64 species. We found that SSD was correlated with the sex difference in the opportunity for sexual selection but not with the sex difference in the Bateman gradient. These findings suggest that pre-copulatory sexual selection plays a limited role for the evolution of sexual size dimorphism in a broad phylogenetic context.

A Life-History Perspective On Sexual Selection in a Polygamous Species

Background: Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we hypothesize that in polygamous species these roles change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis by assessing fitness costs and benefits of multiple matings in both males and females in a polygamous moth species, as in moths not males but females are the signalers and males are the responders. Results: We found that multiple matings confer fitness costs and benefits for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but only 67 % of the males and 14 % of the females mated successfully in all five nights. In addition, the female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, more than 3 matings decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings. Conclusion: Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.

A Life-History Perspective on Sexual Selection in a Polygamous Species

Background: Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we hypothesize that in polygamous species these roles change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis by assessing fitness costs and benefits of multiple matings in both males and females in a polygamous moth species, as in moths not males but females are the signalers and males are the responders. Results: We found that multiple matings confer fitness costs and benefits for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but only 67 % of the males and 14 % of the females mated successfully in all five nights. In addition, the female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, more than 3 matings decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings. Conclusion: Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.

Strong sexual selection despite spatial constraints on extrapair paternity

Extrapair paternity should contribute to sexual selection by increasing the number of potential mates available to each individual. Potential copulation partners are, however, limited by their proximity. Spatial constraints may therefore reduce the impact of extrapair paternity on sexual selection. We tested the effect of spatial constraints on sexual selection by simulating extrapair copulations for 15 species of socially monogamous songbirds with varying rates of extrapair paternity. We compared four metrics of sexual selection between simulated populations without spatial constraints and populations where extrapair copulations were restricted to first- and second-order neighbors. Counter to predictions, sexual selection as measured by the Bateman gradient (the association between the number of copulation partners and offspring produced) increased under spatial constraints. In these conditions, repeated extrapair copulations between the same individuals led to more offspring per copulation partner. In contrast, spatial constraints did somewhat reduce sexual selection—as measured by the opportunity for selection, s’max, and the selection gradient on male quality—when the association between simulated male quality scores and copulation success (e.g., female preferences or male–male competition) was strong. Sexual selection remained strong overall in those populations even under spatial constraints. Spatial constraints did not substantially reduce sexual selection when the association between male quality and copulation success was moderate or weak. Thus, spatial constraints on extrapair copulations are insufficient to explain the absence of strong selection on male traits in many species.

A LIFE-HISTORY PERSPECTIVE ON SEXUAL SELECTION IN A POLYGAMOUS SPECIES

Background Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we argue that in polygamous species these roles may change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis using a polygamous moth species, as in moths not males but females are the signalers and males are the responders. Results We found that multiple matings are beneficial as well as costly for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but when paired with a new virgin mate every night for five nights, only 67% of the males and 14% of the females mated successfully in all five nights. The female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, additional matings beyond 3 decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings. Conclusion Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.

Towards a predictive conservation biology: the devil is in the behaviour

One of the most important challenges in conservation biology is to predict the viability of populations of vulnerable and threatened species. This requires that the demographic stochasticity strongly affecting the ecological and evolutionary dynamics of especially small populations is correctly estimated and modelled. Here, we summarize theoretical evidence showing that the demographic variance in population dynamics is a key parameter determining the probability of extinction and also is directly linked to the magnitude of the genetic drift in the population. The demographic variance is dependent on the mating system, being larger in a polygynous than in monogamous populations. Understanding factors affecting intersexual differences in mating success is therefore essential in explaining variation in the demographic variance. We hypothesize that the strength of sexual selection, for example, quantified by the Bateman gradient, may be a useful predictor of the magnitude of the demographic stochasticity and hence the genetic drift in the population. We provide results from a field study of moose that support this claim. Thus, including central principles from behavioural ecology may increase the reliability of population viability analyses through an improvement of our understanding of factors affecting stochastic influences on population dynamics and evolutionary processes. This article is part of the theme issue ‘Linking behaviour to dynamics of populations and communities: application of novel approaches in behavioural ecology to conservation’.

Structure of sexual networks determines the operation of sexual selection

Sexual selection is a fundamental evolutionary process but remains debated, particularly in the complexity of polyandrous populations where females mate with multiple males. This lack of resolution is partly because studies have largely ignored the structure of the sexual network, that is, the pattern of mate sharing. Here, we quantify what we call mating assortment with network analysis to specify explicitly the indirect as well as direct relationships between partners. We first review empirical studies, showing that mating assortment varies considerably in nature, due largely to basic properties of the sexual network (size and density) and partly to nonrandom patterns of mate sharing. We then use simulations to show how variation in mating assortment interacts with population-level polyandry to determine the strength of sexual selection on males. Controlling for average polyandry, positive mating assortment, arising when more polygynous males tend to mate with more polyandrous females, drastically decreases the intensity of precopulatory sexual selection on male mating success (Bateman gradient) and the covariance between male mating success and postcopulatory paternity share. Average polyandry independently weakened some measures of sexual selection and crucially also impacted sexual selection indirectly by constraining mating assortment through the saturation of the mating network. Mating assortment therefore represents a key—albeit overlooked—modulator of the strength of sexual selection. Our results show that jointly considering sexual network structure and average polyandry more precisely describes the strength of sexual selection.

A rigorous comparison of sexual selection indexes via simulations of diverse mating systems

Sexual selection is a cornerstone of evolutionary theory, but measuring it has proved surprisingly difficult and controversial. Various proxy measures—e.g., the Bateman gradient and the opportunity for sexual selection—are widely used in empirical studies. However, we do not know how reliably these measures predict the strength of sexual selection across natural systems, and most perform poorly in theoretical worst-case scenarios. Here we provide a rigorous comparison of eight commonly used indexes of sexual selection. We simulated 500 biologically plausible mating systems, based on the templates of five well-studied species that cover a diverse range of reproductive life histories. We compared putative indexes to the actual strength of premating sexual selection, measured as the strength of selection on a simulated “mating trait.” This method sidesteps a key weakness of empirical studies, which lack an appropriate yardstick against which proxy measures can be assessed. Our model predicts that, far from being useless, the best proxy measures reliably track the strength of sexual selection across biologically realistic scenarios. The maximum intensity of precopulatory sexual selections′max(the Jones index) outperformed all other indexes and was highly correlated with the strength of sexual selection. In contrast, the Bateman gradient and the opportunity for sexual selection were poor predictors of sexual selection, despite their continuing popularity.