Adult sex ratio variation: implications for breeding system evolution

Adult sex ratio (ASR) exhibits immense variation in nature, although neither the causes nor the implications of this variation are fully understood. According to theory, the ASR is expected to influence sex roles and breeding systems, as the rarer sex in the population has more potential partners to mate with than the more common sex. Changes in mate choice, mating systems and parental care suggest that the ASR does influence breeding behaviour, although there is a need for more tests, especially experimental ones. In the context of breeding system evolution, the focus is currently on operational sex ratios (OSRs). We argue that the ASR plays a role of similar importance and urge researchers to study the ASR and the OSR side by side. Finally, we plead for a dynamic view of breeding system evolution with feedbacks between mating, parenting, OSR and ASR on both ecological and evolutionary time scales.     

Persistence of an extreme male-biased adult sex ratio in a natural population of polyandrous bird

In a number of insects, fishes and birds, the conventional sex roles are reversed: males are the main care provider, whereas females focus on matings. The reversal of typical sex roles is an evolutionary puzzle, because it challenges the foundations of sex roles, sexual selection and parental investment theory. Recent theoretical models predict that biased parental care may be a response to biased adult sex ratios (ASRs). However, estimating ASR is challenging in natural populations, because males and females often have different detectabilities. Here, we use demographic modelling with field data from 2101 individuals, including 579 molecularly sexed offspring, to provide evidence that ASR is strongly male biased in a polyandrous bird with male-biased care. The model predicts 6.1 times more adult males than females (ASR=0.860, proportion of males) in the Kentish plover Charadrius alexandrinus. The extreme male bias is consistent between years and concordant with experimental results showing strongly biased mating opportunity towards females. Based on these results, we conjecture that parental sex-role reversal may occur in populations that exhibit extreme male-biased ASR.     

Sex differences in parental care: Gametic investment,sexual selection,and social environment

Male and female parents often provide different type and amount of care to their offspring. Three major drivers have been proposed to explain parental sex roles: (1) differential gametic investment by males and females that precipitates into sex difference in care, (2) different intensity of sexual selection acting on males and females, and (3) biased social environment that facilitates the more common sex to provide more care. Here, we provide the most comprehensive assessment of these hypotheses using detailed parental care data from 792 bird species covering 126 families. We found no evidence for the gametic investment hypothesis: neither gamete sizes nor gamete production by males relative to females was related to sex difference in parental care. However, sexual selection correlated with parental sex roles, because the male share in care relative to female decreased with both extra‐pair paternity and frequency of male polygamy. Parental sex roles were also related to social environment, because male parental care increased with male‐biased adult sex ratios (ASRs). Taken together, our results are consistent with recent theories suggesting that gametic investment is not tied to parental sex roles, and highlight the importance of both sexual selection and ASR in influencing parental sex roles.     

Parental Care and Mate Choice in the Giant Water Bug Belostoma lutarium

Parental care and sexual selection are highly interrelated. Understanding the evolution of sex‐specific patterns of parental care and sexual selection is a major focus of current evolutionary ecology research and requires empirical studies that simultaneously quantify components of both parental care and sexual selection in a single species. In this study, we quantify the dynamics of paternal care and sexual selection in the giant water bug Belostoma lutarium. Specifically, we examined (1) which sex potentially experiences sexual selection, (2) which traits, if any, are associated with attaining a mate by males and/or females (i.e. which traits are potentially under selection), and (3) which male and female traits, if any, relate to paternal care and offspring survival. Our findings suggest that (1) males are likely the choosier sex and that heavier females are more likely to mate than smaller females, (2) that female body weight is under selection if female weight is a trait that is stable within a given individual and (3) body size is sexually dimorphic, with females being the larger sex in this species. There was no evidence of male or female traits being linked to offspring survival in this species, although this is potentially due to the lack of egg predators in our study. We discuss our findings in relation to the evolution of sex roles and future avenues of research in this species.     

Predicting the direction of sexual selection

Our current understanding of the operation of sexual selection is predicated on a sex difference in parental investment, which favours one sex becoming limiting and choosy over mates, the other competitive and nonchoosy. This difference is reflected in the operational sex ratio (OSR), the ratio of sexually receptive males to females, considered to be of fundamental importance in predicting the direction of sexual selection. Difficulties in measuring OSR directly have led to the use of the potential reproductive rates (PRR) as a measure of the level of investment in offspring of males and females. Several recent studies have emphasized that other factors, such as variation in mate quality and sex differences in mortality patterns, also influence the direction of sexual selection. However, as yet there has been no attempt to form a comprehensive theory of sex roles. Here we show that neither OSR nor PRR is the most fundamentally important determinant of sex roles, and that they are not interchangeable. Instead, the cost of a single breeding attempt has a strong direct effect on competition and choosiness as well as consistent relationships to both OSR and PRR. Our life history based approach to mate choice also yields simple, testable predictions on lack of choice in either sex and on mutual mate choice.     

MUTUAL MATE CHOICE AND SEX DIFFERENCES IN CHOOSINESS

Sexual competition is associated closely with parental care because the sex providing less care has a higher potential rate of reproduction, and hence more to gain from competing for multiple mates. Sex differences in choosiness are not easily explained, however. The lower-caring sex (often males) has both higher costs of choice, because it is more difficult to find replacement mates, and higher direct benefits, because the sex providing more care (usually females) is likely to exhibit more variation in the quality of contributions to the young. Because both the costs and direct benefits of mate choice increase with increasing parental care by the opposite sex, general predictions about sex difference in choosiness are difficult. Furthermore, the level of choosiness of one sex will be influenced by the choosiness of the other. Here, we present an ESS model of mutual mate choice, which explicitly incorporates differences between males and females in life history traits that determine the costs and benefits of choice, and we illustrate our results with data from species with contrasting forms of parental care. The model demonstrates that sex differences in costs of choice are likely to have a much stronger effect on choosiness than are differences in quality variation, so that the less competitive sex will commonly be more choosy. However, when levels of male and female care are similar, differences in quality variation may lead to higher levels of both choice and competition in the same sex.     

Why is mutual mate choice not the norm? Operational sex ratios,sex roles and the evolution of sexually dimorphic and monomorphic signalling.

Biases in the operational sex ratio (OSR) are seen as the fundamental reason behind differential competition for mates in the two sexes, and as a strong determinant behind differences in choosiness. This view has been challenged by Kokko and Monaghan, who argue that sex-specific parental investment, mortalities, mate-encounter rates and quality variation determine the mating system in a way that is not reducible to the OSR. We develop a game-theoretic model of choosiness, signalling and parental care, to examine (i) whether the results of Kokko and Monaghan remain robust when its simplifying assumptions are relaxed, (ii) how parental care coevolves with mating strategies and the OSR and (iii) why mutual mate choice is observed relatively rarely even when both sexes vary in quality. We find qualitative agreement with the simpler approach: parental investment is the primary determinant of sex roles instead of the OSR, and factors promoting choosiness are high species-specific mate-encounter rate, high sex-specific mate-encounter rate, high cost of breeding (parental investment), low cost of mate searching and highly variable quality of the opposite sex. The coevolution of parental care and mating strategies hinders mutual mate choice if one parent can compensate for reduced care by the other, but promotes it if offspring survival depends greatly on biparental care. We argue that the relative rarity of mutual mate choice is not due to biases in the OSR. Instead, we describe processes by which sexual strategies tend to diverge. This divergence is prevented, and mutual mate choice maintained, if synergistic benefits of biparental care render parental investment both high and not too different in the two sexes.     

Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Sex‐biased breeding dispersal is predicted by social environment in birds

Sex‐biased dispersal is common in vertebrates, although the ecological and evolutionary causes of sex differences in dispersal are debated. Here, we investigate sex differences in both natal and breeding dispersal distances using a large dataset on birds including 86 species from 41 families. Using phylogenetic comparative analyses, we investigate whether sex‐biased natal and breeding dispersal are associated with sexual selection, parental sex roles, adult sex ratio (ASR), or adult mortality. We show that neither the intensity of sexual selection, nor the extent of sex bias in parental care was associated with sex‐biased natal or breeding dispersal. However, breeding dispersal was related to the social environment since male‐biased ASRs were associated with female‐biased breeding dispersal. Male‐biased ASRs were associated with female‐biased breeding dispersal. Sex bias in adult mortality was not consistently related to sex‐biased breeding dispersal. These results may indicate that the rare sex has a stronger tendency to disperse in order to find new mating opportunities. Alternatively, higher mortality of the more dispersive sex could account for biased ASRs, although our results do not give a strong support to this explanation. Whichever is the case, our findings improve our understanding of the causes and consequences of sex‐biased dispersal. Since the direction of causality is not yet known, we call for future studies to identify the causal relationships linking mortality, dispersal, and ASR.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

Lonely hearts or sex in the city? Density-dependent effects in mating systems

Two very basic ideas in sexual selection are heavily influenced by numbers of potential mates: the evolution of anisogamy, leading to sex role differentiation, and the frequency dependence of reproductive success that tends to equalize primary sex ratios. However, being explicit about the numbers of potential mates is not typical to most evolutionary theory of sexual selection. Here, we argue that this may prevent us from finding the appropriate ecological equilibria that determine the evolutionary endpoints of selection. We review both theoretical and empirical advances on how population density may influence aspects of mating systems such as intrasexual competition, female choice or resistance, and parental care. Density can have strong effects on selective pressures, whether or not there is phenotypic plasticity in individual strategies with respect to density. Mating skew may either increase or decrease with density, which may be aided or counteracted by changes in female behaviour. Switchpoints between alternative mating strategies can be density dependent, and mate encounter rates may influence mate choice (including mutual mate choice), multiple mating, female resistance to male mating attempts, mate searching, mate guarding, parental care, and the probability of divorce. Considering density-dependent selection may be essential for understanding how populations can persist at all despite sexual conflict, but simple models seem to fail to predict the diversity of observed responses in nature. This highlights the importance of considering the interaction between mating systems and population dynamics, and we strongly encourage further work in this area.     

The role of chemical communication in mate choice

Chemical signals are omnipresent in sexual communication in the vast majority of living organisms. The traditional paradigm was that their main purpose in sexual behaviour was to coordinate mate and species recognition and thus pheromones were conserved in structure and function. In recent years, this view has been challenged by theoretical analyses on the evolution of pheromones and empirical reports of mate choice based on chemical signals. The ability to measure precisely the quantity and quality of chemicals emitted by single individuals has also revealed considerable individual variation in chemical composition and release rates, and there is mounting evidence that prospecting mates respond to this variation. Here, we review the evidence for pheromones as indicators of mate quality and examine the extent of their use in individual mate assessment. We begin by briefly defining the levels of mate choice--species recognition, mate recognition and mate assessment. We then explore the degree to which pheromones satisfy the key criteria necessary for their evolution and maintenance as cues in mate assessment; that is, they should exhibit variation across individuals within a sex and species; they should honestly reflect an individual's quality and thus be costly to produce and/or maintain; they should display relatively high levels of heritability. There is now substantial empirical evidence that pheromones can satisfy all these criteria and, while measurements of the actual metabolic cost of pheromone production remain to some degree lacking, trade-offs between pheromone production and various fitness-related characters such as growth rate, immunocompetence and longevity have been reported for a range of species. In the penultimate section, we outline the growing number of studies where the consequences of chemical-based mate assessment have been investigated, specifically focussing on the reported direct and genetic benefits accrued by the receiver. Finally, we highlight potential areas for future research and in particular emphasise the need for interdisciplinary research that combines exploration of chemical, physiological and behavioural processes to further our understanding of the role of chemical cues in mate assessment.     

Sexual conflict in mammals: consequences for mating systems and life history

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Sex-biased survival predicts adult sex ratio variation in wild birds

Adult sex ratio (ASR) is a central concept in population demography and breeding system evolution, and has implications for population viability and biodiversity conservation. ASR exhibits immense interspecific variation in wild populations, although the causes of this variation have remained elusive. Using phylogenetic analyses of 187 avian species from 59 families, we show that neither hatching sex ratios nor fledging sex ratios correlate with ASR. However, sex-biased adult mortality is a significant predictor of ASR, and this relationship is robust to 100 alternative phylogenetic hypotheses, and potential ecological and life-history confounds. A significant component of adult mortality bias is sexual selection acting on males, whereas increased reproductive output predicts higher mortality in females. These results provide the most comprehensive insights into ASR variation to date, and suggest that ASR is an outcome of selective processes operating differentially on adult males and females. Therefore, revealing the causes of ASR variation in wild populations is essential for understanding breeding systems and population dynamics.     

Multiple paternity is related to adult sex ratio and sex determination system in reptiles

The adult sex ratio (ASR, the proportion of males in the adult population) is an emerging predictor of reproductive behaviour, and recent studies in birds and humans suggest it is a major driver of social mating systems and parental care. ASR may also influence genetic mating systems. For instance male-skewed ASRs are expected to increase the frequency of multiple paternity (defined here as a clutch or litter sired by two or more males) due to higher rates of coercive copulations by males, and/or due to females exploiting the opportunity of copulation with multiple males to increase genetic diversity of their offspring. Here, we evaluate this hypothesis in reptiles that often exhibit high frequency of multiple paternity although its ecological and life-history predictors have remained controversial. Using a comprehensive dataset of 81 species representing all four non-avian reptile orders, we show that increased frequency of multiple paternity is predicted by more male-skewed ASR, and this relationship is robust to simultaneous effects of several life-history predictors. Additionally, we show that the frequency of multiple paternity varies with the sex determination system: species with female heterogamety (ZZ/ZW sex chromosomes) exhibit higher levels of multiple paternity than species with male heterogamety (XY/XX) or temperature-dependent sex determination. Thus, our across-species comparative study provides the first evidence that genetic mating system depends on ASR in reptiles. We call for further investigations to uncover the complex evolutionary associations between mating systems, sex determination systems and ASR.     

Parental and Mating Effort: Is There Necessarily a Trade‐Off?

One of the common assumptions in the study of the evolution of parental care is that trade-offs exist between parental investment and other fitness-related traits. In general, this body of work follows the traditional definition that parental investment (in the current offspring) decreases that individual's ability to invest in future reproduction ( Trivers 1972 ). However, examination of the empirical evidence shows that assuming a trade-off between parental and mating effort is not always appropriate. This overemphasis on a trade-off between mating and parental effort has arisen in part because of an oversimplification of female reproductive strategies, a failure to consider interactions between the sexes, and a tendency to consider behaviours as unifunctional, thereby ignoring the more complex relationship between mating and parental effort in many species. Here, we first examine the empirical evidence for trade-offs between mating and parental effort in males and females to ask when trade-offs occur and what pattern they take. By highlighting a number of exemplar species, we then explore how the presence or absence of trade-offs relates to mate choice and sexual selection in both sexes. Finally, we highlight the importance of considering individual variation, which has been particularly overlooked in examinations of female investment, and how preferences in one sex may influence the existence and our interpretation of apparent trade-offs in the other sex.     

A Cost of Sexual Attractiveness to High-Fitness Females

Adaptive mate choice by females is an important component of sexual selection in many species. The evolutionary consequences of male mate preferences, however, have received relatively little study, especially in the context of sexual conflict, where males often harm their mates. Here, we describe a new and counterintuitive cost of sexual selection in species with both male mate preference and sexual conflict via antagonistic male persistence: male mate choice for high-fecundity females leads to a diminished rate of adaptive evolution by reducing the advantage to females of expressing beneficial genetic variation. We then use a Drosophila melanogaster model system to experimentally test the key prediction of this theoretical cost: that antagonistic male persistence is directed toward, and harms, intrinsically higher-fitness females more than it does intrinsically lower-fitness females. This asymmetry in male persistence causes the tails of the population''s fitness distribution to regress towards the mean, thereby reducing the efficacy of natural selection. We conclude that adaptive male mate choice can lead to an important, yet unappreciated, cost of sex and sexual selection.     

Sex‐related variation in migration phenology in relation to sexual dimorphism: a test of competing hypotheses for the evolution of protandry

Timing of arrival/emergence to the breeding grounds is under contrasting natural and sexual selection pressures. Because of differences in sex roles and physiology, the balance between these pressures on either sex may differ, leading to earlier male (protandry) or female (protogyny) arrival. We test several competing hypotheses for the evolution of protandry using migration data for 22 bird species, including for the first time several monochromatic ones where sexual selection is supposedly less intense. Across species, protandry positively covaried with sexual size dimorphism but not with dichromatism. Within species, there was weak evidence that males migrate earlier because, being larger, they are less susceptible to adverse conditions. Our results do not support the ‘rank advantage’ and the ‘differential susceptibility’ hypotheses, nor the ‘mate opportunity’ hypothesis, which predicts covariation of protandry with dichromatism. Conversely, they are compatible with ‘mate choice’ arguments, whereby females use condition‐dependent arrival date to assess mate quality.     

The evolution and significance of male mate choice

The distinct reproductive roles of males and females, which for many years were characterised in terms of competitive males and choosy females, have remained a central focus of sexual selection since Darwin's time. Increasing evidence now shows that males can be choosy too, even in apparently unexpected situations, such as under polygyny or in the absence of male parental care. Here, we provide a synthesis of the theory on male mate choice and examine the factors that promote or constrain its evolution. We also discuss the evolutionary significance of male mate choice and the contrasts in male versus female mate choice. We conclude that mate choice by males is potentially widespread and has a distinct role in how mating systems evolve.     

Unifying cornerstones of sexual selection: operational sex ratio,Bateman gradient and the scope for competitive investment

What explains variation in the strength of sexual selection across species, populations or differences between the sexes? Here, we show that unifying two well‐known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection. The Bateman gradient and the operational sex ratio (OSR) are incomplete in complementary ways: the former describes the fitness gain per mating and the latter the potential difficulty of achieving it. We combine this insight with an analysis of the scope for sexually selected traits to spread despite naturally selected costs. We explain why the OSR sometimes does not affect the strength of sexual selection. An explanation of sexual selection becomes more logical when a long ‘dry time’ (‘time out’, recovery after mating due to e.g. parental care) is understood to reduce the expected time to the next mating when in the mating pool (i.e. available to mate again). This implies weaker selection to shorten the wait. An integrative view of sexual selection combines an understanding of the origin of OSR biases with how they are reflected in the Bateman gradient, and how this can produce selection for mate acquisition traits despite naturally selected costs.