Sex roles and sex ratios in animals

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.     

Mate location, antennal morphology, and ecology in two praying mantids (Insecta: Mantodea)

The sensory systems employed by animals to locate potential mates are diverse. Among insects, chemical and acoustic signals are commonly used over long distances, with visual signals playing a role in close-range orientation and courtship. Within groups that exhibit a scramble competition mating system, selection on mate searching ability will be particularly strong. Clearly, aspects of the species ecology, such as habitat complexity and population density, will be crucial in the evolution of mate searching systems and sexual signals. Praying mantids exhibit both chemical and visual sexual signalling behaviour, and also vary in their ecology. This study employs scanning electron microscopy of antennal sensory morphology and behavioural assays to investigate the relative importance of chemical and visual signalling in two Australian praying mantid species: Pseudomantis albofimbriata and Ciulfina biseriata . As predicted, the high level of habitat complexity, low population density and strong male dispersal capability of P. albofimbriata corresponded to the use of airborne sex pheromones. Conversely, the open habitat, high population density, and poor dispersal of C. biseriata corresponded to a greater reliance on short-range visual cues for mate location.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 307–313.     

Front Cover

In most animals, competition for mating opportunities is higher among males, whereas females are more likely to provide parental care. In few species, though, these "conventional" sex roles are reversed such that females compete more strongly for matings and males provide most or all parental care. This "reversal" in sex roles is often combined with classical polyandry—a mating system in which a female forms a harem with several males. Here, we review the major hypotheses relating such role reversals to evolutionary and behavioural traits (anisogamy, phylogenetic history, sexy males, parental care, genetic paternity, trade‐off between mating and parenting, adult sex ratio) and to ecological factors (food supply, offspring predation). We evaluate each hypothesis in relation to coucals (Centropodinae), a group of nesting cuckoos of great interest for mating system and parental care theory. The black coucal (Centropus grillii) is the only known bird combining classical polyandry with altricial development of young, a costly trait with regard to parental care. Our long‐term study offers a unique possibility to compare the strongly polyandrous black coucal with a monogamous close relative breeding in the same area and habitat, the white‐browed coucal (C. superciliosus). We show that the evolution of sex roles in coucals and other animals has many different facets. Whereas phylogenetic constraints are important, confidence in genetic paternity is not. In combination with facilitating ecological conditions, adult sex ratios are key to understanding sex roles in coucals, shorebirds, and most likely also other animals. We plead for more studies including experimental tests to understand how biased adult sex ratios emerge and whether they drive sexual selection or vice versa. How do sex ratios and sexual selection interact and feedback on each other? Answers to these questions will be fundamental for understanding the evolution of sex roles in mating and parenting in coucals and other species.     

Are parental care trade‐offs in shorebirds driven by parental investment or sexual selection?

Sexual selection, mating systems and parental behaviour are closely linked, although the exact nature of their relationship is controversial. The parental investment hypothesis (PIH) states that parental care disparity drives sexual selection intensity, because the sex providing less care competes for the sex that provides more. In contrast, the sexual selection hypothesis (SSH) asserts that more intense sexual selection on males leads to reduced male parental investment. We tested these hypotheses using directional phylogenetic comparative methods in shorebirds, which have an unusually diverse array of breeding systems. Changes in parental care and sexual selection intensity were tightly correlated, and we carried out three sets of analyses focusing on changes in male behaviour, female behaviour and in either sex. The results from the analyses were consistent with both PIH and SSH, although the patterns in male transition were sensitive to model values. We propose two explanations for these results. First, phylogenetic transitions may be idiosyncratic so that they depend on the ecological circumstances of individual species. Second, transitions in social traits, such as breeding systems, may be rapid and take place in ecological time, so directional phylogenetic methods that work through longer time scales may not infer accurately the timing and direction of all changes.     

Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish

Sex ratio and sexual dimorphism have long been of interest in population and evolutionary ecology, but consequences for communities and ecosystems remain untested. Sex ratio could influence ecological conditions whenever sexual dimorphism is associated with ecological dimorphism in species with strong ecological interactions. We tested for ecological implications of sex ratio variation in the sexually dimorphic western mosquitofish, Gambusia affinis. This species causes strong pelagic trophic cascades and exhibits substantial variation in adult sex ratios. We found that female-biased populations induced stronger pelagic trophic cascades compared with male-biased populations, causing larger changes to key community and ecosystem responses, including zooplankton abundance, phytoplankton abundance, productivity, pH and temperature. The magnitude of such effects indicates that sex ratio is important for mediating the ecological role of mosquitofish. Because both sex ratio variation and sexual dimorphism are common features of natural populations, our findings should encourage broader consideration of the ecological significance of sex ratio variation in nature, including the relative contributions of various sexually dimorphic traits to these effects.     

被子植物性系统及其可塑性

繁殖是生物适合度的最终表现,有性繁殖相关性状的多态性极大地促进了物种分化和生物多样性的维持,并影响着植物对环境变化的响应。在种群水平上,被子植物的花有雌花、雄花和两性花三种性表型,三种性表型在种群中的分布和频率即定义了种群的性系统。被子植物的性系统包含植物影响性分配和交配的相关特性,决定着雌配子、雄配子在种群中的频率、交配机会及交配方式,是有性繁殖的关键性状,在被子植物中表现出丰富的多态性,在种群水平上分为性单态和性多态两大类。性单态为被子植物的古老性状,而性多态在100多个被子植物科中独立进化产生。被子植物性系统多态性及其变化机理一直是进化生物学与生态学的热点问题之一。该文以种群水平的性多态为对象,总结了被子植物性系统的类型、表达的遗传基础、分布频率,以及遗传因子、非生物环境和交配环境对性系统表达和性分配的影响。     

Sexual conflict in a changing environment

Sexual conflict has extremely important consequences for various evolutionary processes including its effect on local adaptation and extinction probability during environmental change. The awareness that the intensity and dynamics of sexual conflict is highly dependent on the ecological setting of a population has grown in recent years, but much work is yet to be done. Here, we review progress in our understanding of the ecology of sexual conflict and how the environmental sensitivity of such conflict feeds back into population adaptivity and demography, which, in turn, determine a population's chances of surviving a sudden environmental change. We link two possible forms of sexual conflict – intralocus and interlocus sexual conflict – in an environmental context and identify major gaps in our knowledge. These include sexual conflict responses to fluctuating and oscillating environmental changes and its influence on the interplay between interlocus and intralocus sexual conflict, among others. We also highlight the need to move our investigations into more natural settings and to investigate sexual conflict dynamics in wild populations.     

FITNESS CONSEQUENCES OF SEX‐SPECIFIC SELECTION

Theory suggests that sex‐specific selection can facilitate adaptation in sexually reproducing populations. However, sexual conflict theory and recent experiments indicate that sex‐specific selection is potentially costly due to sexual antagonism: alleles harmful to one sex can accumulate within a population because they are favored in the other sex. Whether sex‐specific selection provides a net fitness benefit or cost depends, in part, on the relative frequency and strength of sexually concordant versus sexually antagonistic selection throughout a species’ genome. Here, we model the net fitness consequences of sex‐specific selection while explicitly considering both sexually concordant and sexually antagonistic selection. The model shows that, even when sexual antagonism is rare, the fitness costs that it imposes will generally overwhelm fitness benefits of sexually concordant selection. Furthermore, the cost of sexual antagonism is, at best, only partially resolved by the evolution of sex‐limited gene expression. To evaluate the key parameters of the model, we analyze an extensive dataset of sex‐specific selection gradients from wild populations, along with data from the experimental evolution literature. The model and data imply that sex‐specific selection may likely impose a net cost on sexually reproducing species, although additional research will be required to confirm this conclusion.     

Evolution of sexual size dimorphism in birds: test of hypotheses using blue tits in contrasted Mediterranean habitats

Many hypotheses, either sex‐related or environment‐related, have been proposed to explain sexual size dimorphism in birds. Two populations of blue tits provide an interesting case study for testing these hypotheses because they live in contrasting environments in continental France and in Corsica and exhibit different degree of sexual size dimorphism. Contrary to several predictions, the insular population is less dimorphic than the continental one but neither the sexual selection hypothesis nor the niche variation hypothesis explain the observed patterns. In the mainland population it is advantageous for both sexes to be large, and males are larger than females. In Corsica, however, reproductive success was greater for pairs in which the male was relatively small, i.e. pairs in which sexual size dimorphism is reduced. The most likely explanation is that interpopulation differences in sexual size dimorphism are determined not by sex‐related factors, but by differences in sex‐specific reproductive roles and responses to environmental factors. Because of environmental stress on the island as a result of food shortage and high parasite infestations, the share of parents in caring for young favours small size in males so that a reduced sexual size dimorphism is not the target of selection but a by‐product of mechanisms that operate at the level of individual sexes.     

Sexual differences and sex ratios of dioecious plants under stressful environments

雌雄异株植物对环境胁迫响应的性别差异与性别比例 雌雄异株植物在性特征(繁殖器官)和次级性特征(植物的特征)均表现出性二态。形态、生理与生态特征等次级性特征的性别差异,通常在繁殖成本和其他功能性状之间存在着权衡。尽管有证据表明性二态对环境胁迫的响应不一定存在于所有植物中,但次级性特征的权衡可能受到环境胁迫的影响。当植物表现出性二态时,不同的物种与胁迫因子可以导致性别特异性的响应。因此,胁迫作用对雌雄异株植物影响的概括性研究是必须的。另外,性二态可能会影响雌雄异株植物沿着环境梯度的频率和分布,引起生态位分化与性别空间分异。目前,控制性别比例偏差的原因和机制还知之甚少。本综述旨在讨论不利环境下的性别特异性响应与性别比例偏差,有利于深入的理解性二态对环境胁迫的响应。     

Brain size affects responsiveness in mating behaviour to variation in predation pressure and sex ratio

Despite ongoing advances in sexual selection theory, the evolution of mating decisions remains enigmatic. Cognitive processes often require simultaneous processing of multiple sources of information from environmental and social cues. However, little experimental data exist on how cognitive ability affects such fitness‐associated aspects of behaviour. Using advanced tracking techniques, we studied mating behaviours of guppies artificially selected for divergence in relative brain size, with known differences in cognitive ability, when predation threat and sex ratio was varied. In females, we found a general increase in copulation behaviour in when the sex ratio was female biased, but only large‐brained females responded with greater willingness to copulate under a low predation threat. In males, we found that small‐brained individuals courted more intensively and displayed more aggressive behaviours than large‐brained individuals. However, there were no differences in female response to males with different brain size. These results provide further evidence of a role for female brain size in optimal decision‐making in a mating context. In addition, our results indicate that brain size may affect mating display skill in male guppies. We suggest that it is important to consider the association between brain size, cognitive ability and sexual behaviour when studying how morphological and behavioural traits evolve in wild populations.     

Environmental stressors affect sex ratios in sexually dimorphic plant sexual systems

• Revealing the environmental pressures determining the frequency of females amongst populations of sexually dimorphic plants is a key research question. Analyses of sex ratio variation have been mainly done in dioecious plants, which misses key plant sexual systems that might represent intermediate stages in the evolution of dioecy from hermaphroditism.
• We investigated female frequency across populations of sexually dimorphic plant species in relation to environmental stressors (temperature, precipitation), totaling 342 species, 2011 populations, representing 40 orders and three different sexual systems (dioecy, gynodioecy and subdioecy). We also included the biome where the population was located to test how female frequency may vary more broadly with climate conditions.
• After correcting for phylogeny, our results for gynodioecious systems showed a positive relationship between female frequency and increased environmental stress, with the main effects being temperature‐related. Subdioecious systems also showed strong positive relationships with temperature, and positive and negative relationships related to precipitation, while no significant effects on sex ratio in dioecious plants were detected.
• Combined, we show that female frequencies in an intermediate sexual system on the pathway from hermaphroditism to dioecy respond strongly to environmental stressors and have different selective agents driving female frequency.

     

Neural mechanisms underlying sex-specific behaviors in vertebrates

From invertebrates to humans, males and females of a given species display identifiable differences in behaviors, mostly but not exclusively pertaining to sexual and social behaviors. Within a species, individuals preferentially exhibit the set of behaviors that is typical of their sex. These behaviors include a wide range of coordinated and genetically pre-programmed social and sexual displays that ensure successful reproductive strategies and the survival of the species. What are the mechanisms underlying sex-specific brain function? Although sexually dimorphic behaviors represent the most extreme examples of behavioral variability within a species, the basic principles underlying the sex specificity of brain activity are largely unknown. Moreover, with few exceptions, the quest for fundamental differences in male and female brain structures and circuits that would parallel that of sexual behaviors and peripheral organs has so far uncovered modest quantitative rather than the expected clear qualitative differences. As will be detailed in this review, recent advances have directly challenged the established notion of the unique role of steroid hormones in organizing and activating male- and female-specific brain circuits and have uncovered new mechanisms underlying the neural control of sex-specific behaviors.     

HOMAGE TO BATEMAN: SEX ROLES PREDICT SEX DIFFERENCES IN SEXUAL SELECTION

Classic sex role theory predicts that sexual selection should be stronger in males in taxa showing conventional sex roles and stronger in females in role reversed mating systems. To test this very central prediction and to assess the utility of different measures of sexual selection, we estimated sexual selection in both sexes in four seed beetle species with divergent sex roles using a novel experimental design. We found that sexual selection was sizeable in females and the strength of sexual selection was similar in females and males in role‐reversed species. Sexual selection was overall significantly stronger in males than in females and residual selection formed a substantial component of net selection in both sexes. Furthermore, sexual selection in females was stronger in role‐reversed species compared to species with conventional sex roles. Variance‐based measures of sexual selection (the Bateman gradient and selection opportunities) were better predictors of sexual dimorphism in reproductive behavior and morphology across species compared to trait‐based measures (selection differentials). Our results highlight the importance of using assays that incorporate components of fitness manifested after mating. We suggest that the Bateman gradient is generally the most informative measure of the strength of sexual selection in comparisons across sexes and/or species.     

Evolutionary pathways in shorebird breeding systems: sexual conflict, parental care, and chick development

Sexual selection, mating opportunities, and parental behavior are interrelated, although the specific nature of these relationships is controversial. Two major hypotheses have been suggested. The parental investment hypothesis states that the relative parental investment of the sexes drives the operation of sexual selection. Thus, the sex that invests less in offspring care competes more intensely and monopolizes access to mates. The sexual conflict hypothesis proposes that sexual selection (the competition among both males and females for mates), mating opportunities, and parental behavior are interrelated and predicts a feedback loop between mating systems and parental care. Here we test both hypotheses using a comprehensive dataset of shorebirds, a maximum-likelihood statistical technique, and a recent supertree of extant shorebirds and allies. Shorebirds are an excellent group for these analyses because they display unique variation in parental care and social mating system. First, we show that chick development constrains the evolution of both parental care and mate competition, because transitions toward more precocial offspring preceded transitions toward reduced parental care and social polygamy. Second, changes in care and mating systems respond to one another, most likely because both influenced and are influenced by mating opportunities. Taken together, our results are more consistent with the sexual conflict hypothesis than the parental investment hypothesis.     

Polyandry and alternative mating tactics

Many species in the animal kingdom are characterized by alternative mating tactics (AMTs) within a sex. In males, such tactics include mate guarding versus sneaking behaviours, or territorial versus female mimicry. Although AMTs can occur in either sex, they have been most commonly described in males. This sex bias may, in part, reflect the increased opportunity for sexual selection that typically exists in males, which can result in a higher probability that AMTs evolve in that sex. Consequently, females and polyandry can play a pivotal role in governing the reproductive success associated with male AMTs and in the evolutionary dynamics of the tactics. In this review, we discuss polyandry and the evolution of AMTs. First, we define AMTs and review game theoretical and quantitative genetic approaches used to model their evolution. Second, we review several examples of AMTs, highlighting the roles that genes and environment play in phenotype expression and development of the tactics, as well as empirical approaches to differentiating among the mechanisms. Third, ecological and genetic constraints to the evolution of AMTs are discussed. Fourth, we speculate on why female AMTs are less reported on in the literature than male tactics. Fifth, we examine the effects of AMTs on breeding outcomes and female fitness, and as a source, and possibly also a consequence, of sexual conflict. We conclude by suggesting a new model for the evolution of AMTs that incorporates both environmental and genetic effects, and discuss some future avenues of research.     

Is sexual segregation in the guppy, <Emphasis Type="Italic">Poecilia reticulata</Emphasis>, consistentwith the predation risk hypothesis?

We examined the importance of sex differences in predation risk in generating sexual segregation in the guppy, Poecilia reticulata. We hypothesised that sex differences in predation risk will result in habitat segregation and ultimately social segregation of the sexes, with the more vulnerable sex (males in this case) using safer habitats. In accordance with the predation risk hypothesis we observed sexual segregation in a population associated with high but not low predation risk. Under high predation risk we observed a larger proportion of males in shallow marginal habitats resulting in habitat segregation and ultimately social segregation of the sexes. Furthermore, habitat segregation by sex was associated with habitat segregation by body length with shoals in deeper water having a larger mean body length. Shoaling fish species have been key models in investigating group living, and further research directed towards understanding sexual segregation in other fish species would be valuable.     

The ecology of sexual conflict: ecologically dependent parallel evolution of male harm and female resistance in Drosophila melanogaster

The prevalence of sexual conflict in nature, along with the potentially stochastic nature of the resulting coevolutionary trajectories, makes it an important driver of phenotypic divergence and speciation that can operate even in the absence of environmental differences. The majority of empirical work investigating sexual conflict's role in population divergence/speciation has therefore been done in uniform environments and any role of ecology has largely been ignored. However, theory suggests that natural selection can constrain phenotypes influenced by sexual conflict. We use replicate populations of Drosophila melanogaster adapted to alternative environments to test how ecology influences the evolution of male effects on female longevity. The extent to which males reduce female longevity, as well as female resistance to such harm, both evolved in association with adaptation to the different environments. Our results demonstrate that ecology plays a central role in shaping patterns of population divergence in traits under sexual conflict.     

Body size and sexual size dimorphism in primates: influence of climate and net primary productivity

Understanding the evolution of body size and sexual size dimorphism has been a longstanding goal in evolutionary biology. Previous work has shown that environmental stress can constrain male‐biased sexual size dimorphism at the population level, but we know little about how this might translate to geographical patterns of body size and sexual size dimorphism at the species level. Environmental constraints due to a highly seasonal, resource‐poor and/or variable environment have often been cited to explain the unusual lack of sexual size dimorphism among Madagascar's diverse and numerous primate taxa; however, empirical tests of this hypothesis are lacking. Using a phylogenetic approach and a geographical information system platform, we explored the role of seasonality, interannual variability and annual measures of temperature and rainfall, and net primary productivity on patterns of body size and sexual size dimorphism across 130 species of primates. Phylogenetically controlled comparisons showed no support for a role of environmental constraints in moderating sexual size dimorphism at the interspecific level, despite significant associations of environmental variables with body mass. Results suggest that the focus of discussions that have dominated in the last two decades regarding the role of environmental constraints in driving patterns of monomorphism of Madagascar's lemurs should be reconsidered; however, the conundrum remains.