Sperm Sociality: Cooperation, Altruism, and Spite

The idea of subfertile or altogether infertile sperm seems an evolutionary paradox, so why have they evolved in a diverse set of species, from molluscs to mice? Understanding sperm sociality may provide the answer

Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus

When females are sexually promiscuous, sexual selection continues after insemination through sperm competition and cryptic female choice, and male traits conveying an advantage in competitive fertilization are selected for. Although individual male and ejaculate traits are known to influence paternity in a competitive scenario, multiple mechanisms co-occur and interact to determine paternity. The way in which different traits interact with each other and the mechanisms through which their heritability is maintained despite selection remain unresolved. In the promiscuous fowl, paternity is determined by the number of sperm inseminated into a female, which is mediated by male social dominance, and by the quality of the sperm inseminated, measured as sperm mobility. Here we show that: (i) the number of sperm inseminated determines how many sperm reach the female sperm-storage sites, and that sperm mobility mediates the fertilizing efficiency of inseminated sperm, mainly by determining the rate at which sperm are released from the female storage sites, (ii) like social status, sperm mobility is heritable, and (iii) subdominant males are significantly more likely to have higher sperm mobility than dominant males. This study indicates that although the functions of social status and sperm mobility are highly interdependent, the lack of phenotypic integration of these traits may maintain the variability of male fitness and heritability of fertilizing efficiency

Sexual selection in complex communities : integrating interspecific reproductive interference in structured populations

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 PDFPeer reviewe

Differential female sociality is linked with the fine-scale structure of sexual interactions in replicate groups of red junglefowl, Gallus gallus

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

Meta-analysis shows no consistent evidence for senescence in ejaculate traits across animals

Male reproductive traits such as ejaculate size and quality, are expected to decline with advancing age due to senescence. It is however unclear whether this expectation is upheld across taxa. We perform a meta-analysis on 379 studies, to quantify the effects of advancing male age on ejaculate traits across 157 species of non-human animals. Contrary to predictions, we find no consistent pattern of age-dependent changes in ejaculate traits. This result partly reflects methodological limitations, such as studies sampling a low proportion of adult lifespan, or the inability of meta-analytical approaches to document non-linear ageing trajectories of ejaculate traits; which could potentially lead to an underestimation of senescence. Yet, we find taxon-specific differences in patterns of ejaculate senescence. For instance, older males produce less motile and slower sperm in ray-finned fishes, but larger ejaculates in insects, compared to younger males. Notably, lab rodents show senescence in most ejaculate traits measured. Our study challenges the notion of universal reproductive senescence, highlighting the need for controlled methodologies and a more nuanced understanding of reproductive senescence, cognisant of taxon-specific biology, experimental design, selection pressures, and life-history

Sex-specific responses to sexual familiarity, and the role of olfaction in

Studies of mating preferences have largely neglected the potential effects of individuals encountering their previous mates ('directly sexually familiar'), or new mates that share similarities to previous mates, e.g. from the same family and/or environment ('phenotypically sexually familiar'). Here, we show that male and female Drosophila melanogaster respond to the direct and phenotypic sexual familiarity of potential mates in fundamentally different ways. We exposed a single focal male or female to two potential partners. In the first experiment, one potential partner was novel (not previously encountered) and one was directly familiar (their previous mate); in the second experiment, one potential partner was novel (unrelated, and from a different environment from the previous mate) and one was phenotypically familiar (from the same family and rearing environment as the previous mate). We found that males preferentially courted novel females over directly or phenotypically familiar females. By contrast, females displayed a weak preference for directly and phenotypically familiar males over novel males. Sex-specific responses to the familiarity of potential mates were significantly weaker or absent in Orco 1 mutants, which lack a co-receptor essential for olfaction, indicating a role for olfactory cues in mate choice over novelty. Collectively, our results show that direct and phenotypic sexual familiarity is detected through olfactory cues and play an important role in sex-specific sexual behaviour

Temporal dynamics of competitive fertilization in social groups of red junglefowl (Gallus gallus) shed new light on avian sperm competition

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'

Endless forms of sexual selection

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a "stock-taking\u27\u27 workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion rather than provide a comprehensive overview of the entire field. These questions are organized into four thematic sections we deem essential to the field. First we focus on the evolution of mate choice and mating systems. Variation in mate quality can generate both competition and choice in the opposite sex, with implications for the evolution of mating systems. Limitations on mate choice may dictate the importance of direct vs. indirect benefits in mating decisions and consequently, mating systems, especially with regard to polyandry. Second, we focus on how sender and receiver mechanisms shape signal design. Mediation of honest signal content likely depends on integration of temporally variable social and physiological costs that are challenging to measure. We view the neuroethology of sensory and cognitive receiver biases as the main key to signal form and the \u27aesthetic sense\u27 proposed by Darwin. Since a receiver bias is sufficient to both initiate and drive ornament or armament exaggeration, without a genetically correlated or even coevolving receiver, this may be the appropriate \u27null model\u27 of sexual selection. Thirdly, we focus on the genetic architecture of sexually selected traits. Despite advances in modern molecular techniques, the number and identity of genes underlying performance, display and secondary sexual traits remains largely unknown. In-depth investigations into the genetic basis of sexual dimorphism in the context of long-term field studies will reveal constraints and trajectories of sexually selected trait evolution. Finally, we focus on sexual selection and conflict as drivers of speciation. Population divergence and speciation are often influenced by an interplay between sexual and natural selection. The extent to which sexual selection promotes or counteracts population divergence may vary depending on the genetic architecture of traits as well as the covariance between mating competition and local adaptation. Additionally, post-copulatory processes, such as selection against heterospecific sperm, may influence the importance of sexual selection in speciation. We propose that efforts to resolve these four themes can catalyze conceptual progress in the field of sexual selection, and we offer potential avenues of research to advance this progress