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Parental care can enhance offspring survival but may impose significant costs to parents. The costs and benefits of care are key to understanding patterns of parental care, where parents can benefit by having their partner increase investment in care, while reducing their own effort. However, investigating the costs and benefits of parental care in wild populations is challenging. Here we use highly detailed behavioral observations in families of a small shorebird, where one parent frequently deserts its offspring, to explore the potential costs and benefits of desertion in a wild population. We first show that females desert their broods more frequently than males. Second, we investigate the benefits of this frequent female desertion in terms of additional mating opportunities, and the costs of desertion to females in terms of the growth and survival of deserted offspring. Our results indicate that female desertion is favored by a combination of remating benefits and a lack of costs to brood growth and survival, as abandoned male parents continue to provide care after desertion. Our results shed light on the costs and benefits underlying natural desertion strategies and suggest that female desertion is a fine-tuned behavior that responds to seasonally changing benefits of desertion.

Pathogen traits can vary greatly and impact the ability of a pathogen to persist in a population. Although this variation is fundamental to disease ecology, little is known about the evolutionary pressures that drive these differences, particularly where they interact with host behavior. We hypothesized that host behaviors relevant to different transmission routes give rise to differences in contact network structure, constraining the space over which pathogen traits can evolve to maximize fitness. Our analysis of 232 contact networks across mammals, birds, reptiles, amphibians, arthropods, fish, and mollusks found that contact network topology varies by contact events, most notably in networks that are representative of fluid-exchange transmission. Using infectious disease model simulations, we showed that these differences in network structure suggest pathogens transmitted through fluid-exchange contact events will need traits associated with high transmissibility to successfully proliferate, compared to pathogens that transmit through other types of contact. These findings were supported through a review of known traits of pathogens that transmit in humans. Our work demonstrates that contact network structure may drive the evolution of compensatory pathogen traits according to transmission strategy, providing essential context for understanding pathogen evolution and ecology.

Despite widespread evidence that mating and intrasexual competition are costly, relatively little is known about how these costs dynamically change male and female phenotypes. Here, we test multiple hypotheses addressing this question in replicate flocks of red junglefowl (Gallus gallus). First, we test the interrelationships between social status, comb size (a fleshy ornament) and body mass at the onset of a mating trial. While comb size covaried positively with body mass across individuals of both sexes, comb size was positively related to social status in females but not in males. Second, we test for changes within individuals in body mass and comb size throughout the mating trial. Both body mass and comb size declined at the end of a trial in both sexes, suggesting that mating effort and exposure to the opposite sex are generally costly. Males lost more body mass if they (a) were socially subordinate, (b) were chased by other males or (c) mated frequently, indicating that subordinate status and mating are independently costly. Conversely, females lost more body mass if they were exposed to a higher frequency of coerced matings, suggesting costs associated with male sexual harassment and female resistance, although costs of mating per se could not be completely ruled out. Neither competitive nor mating interactions predicted comb size change in either sex. Collectively, these results support the notion that sex‐specific costs associated with social status and mating effort result in differential, sex‐specific dynamics of phenotypic change., We present empirical evidence that social status and mating behaviours are associated with sex‐specific dynamic changes in body mass, but not ornament expression, in replicate groups of polygynandrous red junglefowl (Gallus gallus). Photo by Dom Cram.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

1. Despite increasing evidence of the importance of repeatable among-individual differences in behavior (animal personality) in ecology and evolution, little remains known about the role of animal personalities in sexual selection. 2. Here, we present an investigation of the hypothesis that the personalities of individuals and their sexual partners play a role in different episodes of sexual selection, and the extent to which these effects are modulated by the social environment. 3. We first examined how two repeatable behaviors — exploration and boldness — are associated with pre- and postcopulatory sexual selection, with a focus on the former, in male red junglefowl, Gallus gallus, using replicate groups across three experimental sex ratio treatments. We further explored how the social environment modulates relationships between male personality and mating performance, and whether mating is assortative or disassortative with respect to exploration or boldness. Lastly, we examined behavioral mechanisms linking personality with mating performance. 4. Across all sex ratios, the fastest- and slowest-exploring males harassed females proportionally less, and faster-exploring males associated with females more and received more sexual solicitations. In female-biased groups, the fastest- and slowest-exploring males experienced the highest mating success and lowest sperm competition intensity. Faster-exploring males also obtained more mates in female-biased groups when their competitors were, on average, slower-exploring, and the proportion of matings obtained by fast-exploring males decreased with the proportion of fast-exploring males in a group, consistent with negative frequency-dependent sexual selection. While boldness did not predict mating performance, there was a tendency for individuals to mate disassortatively with respect to boldness. 5. Collectively, our results suggest that male exploration can play a role in sexual selection, and that sexual selection on personality is complex and contingent on the social environment.

The social environment is a key factor determining fitness by influencing multiple stages of reproduction, including pair formation, mating behavior and parenting. However, the influence of social structure across different aspects of breeding is rarely examined simultaneously in wild populations. We therefore lack a consolidation of the mechanisms by which sociality impacts reproduction. Here we investigate the implications of the social environment before and during breeding on multiple stages of reproduction in an island population of the ground nesting shorebird, the Kentish plover (Charadrius alexandrinus). We utilise information on mating decisions, nest locations and nesting success across multiple years in combination with social network analysis. Sociality before breeding was connected with patterns of pair formation. In addition, site fidelity and personal breeding experience was associated with the spatial organisation of breeding pairs. Our results provide evidence that, while differential social interactions at localised scales influence patterns of reproductive pairing, site fidelity and personal breeding experience influence the structure of populations at the landscape scale. Our results underline the tight link between the social structure of populations and patterns of mating, while revealing that the relative influence of sociality, breeding experience and local ecology are dynamic across different facets of reproduction.

Halimubieke, Naerhulan et al., When individuals breed more than once, parents are faced with the choice of whether to re-mate with their old partner or divorce and select a new mate. Evolutionary theory predicts that, following successful reproduction with a given partner, that partner should be retained for future reproduction. However, recent work in a polygamous bird, has instead indicated that successful parents divorced more often than failed breeders (Halimubieke et al. in Ecol Evol 9:10734–10745, 2019), because one parent can beneft by mating with a new partner and reproducing shortly after divorce. Here we investigate whether successful breeding predicts divorce using data from 14 well-monitored populations of plovers (Charadrius spp.). We show that successful nesting leads to divorce, whereas nest failure leads to retention of the mate for follow-up breeding. Plovers that divorced their partners and simultaneously deserted their broods produced more ofspring within a season than parents that retained their mate. Our work provides a counterpoint to theoretical expectations that divorce is triggered by low reproductive success, and supports adaptive explanations of divorce as a strategy to improve individual reproductive success. In addition, we show that temperature may modulate these costs and benefts, and contribute to dynamic variation in patterns of divorce across plover breeding systems

A central problem in evolutionary biology is to determine whether and how social interactions contribute to natural selection. This can be addressed with selection analyses that relate individual fitness to individual and social phenotypes. One such approach, known as social selection analysis, leads to the intuitive result that fitness effects from social partners will contribute to selection only if there is a correlation between the traits of individuals and their social partners (non-random phenotypic assortment). However, there have been inconsistencies in the application of this approach that center around the measurement of phenotypic assortment. Here, we use data analysis and simulations to resolve these inconsistencies, showing that: (i) not all measures of assortment are suitable for social selection analysis; and (ii) the interpretation of assortment, and how to detect non-random assortment, will depend on the scale at which it is measured. We discuss links between social selection and kin selection theory, and we provide a practical guide for the social selection approach. This article is protected by copyright. All rights reserved

Recent work indicates that social structure has extensive implications for patterns of sexual selection and sexual conflict. However, little is known about the individual variation in social behaviours linking social structure to sexual interactions. Here, we use network analysis of replicate polygynandrous groups of red junglefowl ( Gallus gallus ) to show that the association between social structure and sexual interactions is underpinned by differential female sociality. Sexual dynamics are largely explained by a core group of highly social, younger females, which are more fecund and more polyandrous, and thus associated with more intense postcopulatory competition for males. By contrast, less fecund females from older cohorts, which tend to be socially dominant, avoid male sexual attention by clustering together and perching on branches, and preferentially reproduce with dominant males by more exclusively associating and mating with them. Collectively, these results indicate that individual females occupy subtly different social niches and demonstrate that female sociality can be an important factor underpinning the landscape of intrasexual competition and the emergent structure of animal societies.

Theory predicts that males will strategically invest in ejaculates according to the value of mating opportunities. While strategic sperm allocation has been studied extensively, little is known about concomitant changes in seminal fluid (SF) and its molecular composition, despite increasing evidence that SF proteins (SFPs) are fundamental in fertility and sperm competition. Here, we show that in male red junglefowl, Gallus gallus, along with changes in sperm numbers and SF investment, SF composition changed dynamically over successive matings with a first female, immediately followed by mating with a second, sexually novel female. The SF proteome exhibited a pattern of both protein depletion and enrichment over successive matings, including progressive increases in immunity and plasma proteins. Ejaculates allocated to the second female had distinct proteomic profiles, where depletion of many SFPs was compensated by increased investment in others. This response was partly modulated by male social status: when mating with the second, novel female, subdominants (but not dominants) preferentially invested in SFPs associated with sperm composition, which may reflect status-specific differences in mating rates, sperm maturation and sperm competition. Global proteomic SF analysis thus reveals that successive matings trigger rapid, dynamic SFP changes driven by a combination of depletion and strategic allocation.

Sexual selection is widely recognized as the evolutionary agent driving male exaggeration and strategies of intrasexual competition over reproductive opportunities. Two advances have characterized the development of our understanding of sexual selection in recent years. The first was the realization that sexual selection can extend to post-copulatory episodes whenever females mate with multiple males (polyandry). The second concerns the operation of sexual selection in structured population in light of increasing evidence that populations are often non-randomly assembled. Populations of domestic fowl (Gallus domesticus) and red junglefowl (Gallus gallus), which are typically socially-structured and polyandrous, have offered a convenient vertebrate model system to study patterns and mechanisms of sexual selection, providing a helpful counterpoint to studies of socially monogamous systems. Here, we review our understanding of the way sexual selection operates in these populations, with emphasis on recent work focusing on the interrelated implications of polyandry and social structure.

Funding: European Research Council (771387) and the Natural Environment Research Council (NE/K009524/1) (AG). The social structure of populations plays a key role in shaping variation in sexual selection. In nature, sexual selection occurs in communities of interacting species; however, heterospecifics are rarely included in characterizations of social structure. Heterospecifics can influence the reproductive outcomes of intrasexual competition by interfering with intraspecific sexual interactions (interspecific reproductive interference [IRI]). We outline the need for studies of sexual selection to incorporate heterospecifics as part of the social environment. We use simulations to show that classic predictions for the effect of social structure on sexual selection are altered by an interaction between social structure and IRI. This interaction has wide‐ranging implications for patterns of sexual conflict and kin‐selected reproductive strategies in socially structured populations. Our work bridges the gap between sexual selection research on social structure and IRI, and highlights future directions to study sexual selection in interacting communities. Publisher PDF

Sexually-selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus any seasonal changes in nutritional quality are predicted to alter the average size of sexually-selected traits as well as the degree of sexual dimorphism in populations. However, while traits affected by mate choice are well-studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually-selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean-scaled evolvability of sexually-selected traits across conditions. Using the insect, Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, we studied the extent to which weapon expression, sexual dimorphism, and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, while those raised on a high quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions. This article is protected by copyright. All rights reserved.

The study of sexual selection is being revolutionised by the realisation that most populations exhibit some degree of polyandry, i.e. females mating with multiple males. Polyandry can drastically change the operation of sexual selection on males as it reduces the reproductive success that males derive by mating with different females, by forcing their ejaculates to compete for fertilisation after copulation (sperm competition). Variation in polyandry within a population means that the impact of polyandry can differ drastically across males, depending on the polyandry of their own mating partners. Because the patterns through which males share mates within a population may have strong repercussions for variation in male reproductive success, measuring such patterns is critical to study the operation of sexual selection. Several methods have been proposed to measure the pattern of mate sharing at the population level. Here, we develop a new method (sperm competition intensity correlation, SCIC) and compare its performance against two established methods (Newman’s assortativity and nestedness), using both idealised model populations and random simulated populations, across a range of biologically relevant population parameters: (i) population size, (ii) sex ratio and (iii) the ‘mating density’ of the population. We conclude that SCIC may be the most promising approach, as it is both internally consistent and robust across the parameter range. We discuss some important caveats and provide advice regarding the choice of method for future studies of sexual selection. Electronic supplementary material The online version of this article (doi:10.1007/s00265-015-2041-7) contains supplementary material, which is available to authorized users.

Studies of birds have made a fundamental contribution to elucidating sperm competition processes, experimentally demonstrating the role of individual mechanisms in competitive fertilization. However, the relative importance of these mechanisms and the way in which they interact under natural conditions remain largely unexplored. Here, we conduct a detailed behavioural study of freely mating replicate groups of red junglefowl, Gallus gallus , to predict the probability that competing males fertilize individual eggs over the course of 10-day trials. Remating frequently with a female and mating last increased a male's probability of fertilization, but only for eggs ovulated in the last days of a trial. Conversely, older males, and those mating with more polyandrous females, had consistently lower fertilization success. Similarly, resistance to a male's mating attempts, particularly by younger females, reduced fertilization probability. After considering these factors, male social status, partner relatedness and the estimated state of male extragonadal sperm reserves did not predict sperm competition outcomes. These results shed new light on sperm competition dynamics in taxa such as birds, with prolonged female sperm storage and staggered fertilizations. This article is part of the theme issue ‘Fifty years of sperm competition’.

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, i.e. 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 non-random 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 challenge in evolutionary biology is to understand the operation of sexual selection on males in polyandrous groups, where sexual selection occurs before and after mating. Here, we combine fine-grained behavioral information (41,000 interactions) with molecular parentage data to study sexual selection in replicated, age-structured groups of polyandrous red junglefowl, Gallus gallus. Male reproductive success was determined by the number of females mated (precopulatory sexual selection) and his paternity share, which was driven by the polyandry of his female partners (postcopulatory sexual selection). Pre- and postcopulatory components of male reproductive success covaried positively; males with high mating success also had high paternity share. Two male phenotypes affected male pre- and postcopulatory performance: average aggressiveness toward rival males and age. Aggressive males mated with more females and more often with individual females, resulting in higher sexual exclusivity. Similarly, younger males mated with more females and more often with individual females, suffering less intense sperm competition than older males. Older males had a lower paternity share even allowing for their limited sexual exclusivity, indicating they may produce less competitive ejaculates. These results show that-in these populations-postcopulatory sexual selection reinforces precopulatory sexual selection, consistently promoting younger and more aggressive males.

Sexual selection is traditionally measured at the population level, assuming that populations lack structure. However, increasing evidence undermines this approach, indicating that intrasexual competition in natural populations often displays complex patterns of spatial and temporal structure. This complexity is due in part to the degree and mechanisms of polyandry within a population, which can influence the intensity and scale of both pre- and post-copulatory sexual competition. Attempts to measure selection at the local and global scale have been made through multi-level selection approaches. However, definitions of local scale are often based on physical proximity, providing a rather coarse measure of local competition, particularly in polyandrous populations where the local scale of pre- and post-copulatory competition may differ drastically from each other. These limitations can be solved by social network analysis, which allows us to define a unique sexual environment for each member of a population: ‘local scale’ competition, therefore, becomes an emergent property of a sexual network. Here, we first propose a novel quantitative approach to measure pre- and post-copulatory sexual selection, which integrates multi-level selection with information on local scale competition derived as an emergent property of networks of sexual interactions. We then use simple simulations to illustrate the ways in which polyandry can impact estimates of sexual selection. We show that for intermediate levels of polyandry, the proposed network-based approach provides substantially more accurate measures of sexual selection than the more traditional population-level approach. We argue that the increasing availability of fine-grained behavioural datasets provides exciting new opportunities to develop network approaches to study sexual selection in complex societies.