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Cephalopods are a remarkable group for studies on sexual selection, due to their complex reproductive behavior, pronounced sexual dimorphism, polygamous behavior, as well as cumulative evidence of pre- and postcopulatory male-male competition and female choice in the group. is paper provides a review of sexual selection studies on cephalopods, with an emphasis on the loliginid squid mating system. In this system, males may adopt alternative reproductive tactics (ART) and display male intrasexual dimorphism, with each morph generally exhibiting distinct behaviors and ejaculate traits. Consort males typically transfer ejaculates to the female mantle cavity, while sneaker males typically transfer ejaculates to the female buccal region, where a sperm storage organ is located. Each site provides distinct fertilization environments for the ejaculates of each morph, differing in the availability of eggs, gamete protection, and timing between mating and fertilization. Accordingly, the ejaculates of each morph show putative adaptations for each site, differing in size, morphology, sperm release duration, and sperm behavior. Although solid evidence is lacking for most loliginids, cryptic female choice may occur in this system through, for example, spermatangia removal or egg string manipulation during fertilization. In addition, recent evidence for one loliginid species indicates that adoption of male ART is ontogenetic and may represent two alternative pathways: from immature males (i) directly to consort phenotype or (ii) going through a sneaker phase, then switching to consort morph. The second pathway would, therefore, imply striking change in behavior, physiology, and ejaculates. Moreover, data on the age of this species suggests that the adoption of sneaker tactic early in life may be associated with extending the male mating period by 25%. With such a peculiar system, loliginids should prove useful not only for comprehending the evolution of female promiscuity and ART in cephalopods, but also as an emerging nonvertebrate and nonarthropod model for testing sperm competition models.

Female promiscuity is a pervasive selective force on male reproductive traits, and the strength of sexual selection is predicted to influence the tradeoff between lifespan and reproduction. In species where sexual selection is intense, males are predicted to invest in sexual strategies that shorten their lifespan, potentially resulting in female-biased sexual dimorphism in longevity. However, comparative analyses have provided contrasting results, potentially due to the use of broad mating system categories or sexual size dimorphism as a proxy for sexual selection. Here, we used female remating rate (i.e., female promiscuity) as a more direct measure of sexual selection strength, and conducted a phylogenetic comparative analysis of the relationship between female remating rate and sexual dimorphism in lifespan in 29 species of Drosophila. We did not find strong evidence that female remating rate was correlated with sexual-dimorphism in lifespan. However, we found that male and female lifespans are positively correlated among species, and that phylogeny and residual variance (i.e., variation in non-phylogenetic factors) are important in determining female remating rate, male and female lifespans separately, and the correlation between male and female lifespan. We suggest that variation in the nature of sexual competition as well as variation between studies could account for some of the unexplained variation among species in the relation between female remating rate and sexual dimorphism in lifespan.

Body and testes size can significantly affect male reproductive success under pre- and post-copulatory sexual selection. Testicular relative mass and/or volume are often used as a characteristic of sperm competitive ability in a comparison of phylogenetically close mammal species. Mus spicilegus males have the largest testes relative to body mass of any Mus species, which is often an indicator of high sperm competition. These findings suggest that these mound-building mice are probably not strictly monogamous. Here, we show the quantitative characteristics of testicular size, variation, and allometry of two sibling species with a different social and mating system, the house mouse (Mus musculus) and the mound-building mouse (M. spicilegus) from the Western Carpathian (Slovakia). We investigated whether testicular size (testicular length/width) was correlated with the head-and-body length and body weight, which are not involved in reproduction. Our results confirmed higher testicular values in M. spicilegus than in M. musculus. Similarly, the high phenotypic variance and positive allometry in testicular growth confirmed the suggestion that males with larger testes and a higher production of testosterone may be more competitive and more successful in post-copulatory selection.

Adaptive explanations for the evolution of extra-pair paternity (EPP) in birds often assume cuckolding males to be better-ornamented than cuckolded males. Several studies have confirmed that either male sexual ornamentation is associated with EPP or that phenotypes of cuckolded and cuckolding males differ. Expression of male ornamentation may change with age; however, a recent meta-analysis has identified age itself as an important factor that differed in cuckolding and cuckolded males. The age of social female partner may also affect EPP, though this has received little attention. Here, by using detailed data on age of individual barn swallows (Hirundo rustica rustica), we identified age as the major predictor of male and female promiscuity. Our results revealed that, whereas a male’s ability to obtain an extra-pair mate increased linearly with age, the only predictor of the probability of a male being cuckolded was the age of his social partner, with older females engaging more frequently in EPP. In contrast, male ornamentation was not significantly related to EPP pattern. Tarsus length was the sole significant phenotypic trait in comparison between cuckolding and cuckolded males. Our data provide little support for the hypothesis that extra-pair mate choice in our barn swallow population was ornament driven. This may indicate either a non-adaptive scenario for EPP, for example with older males better able to coerce females into copulation, or EPP mating based on other than absolute mate-choice criteria associated with the expression of male ornamentation. We analysed patterns of extra-pair paternity (EPP) in barn swallows. Derived from observation of 160 nests, our results appear to differ from the findings of some previous studies that identified ornamental traits as being associated with extra-pair and within-pair paternity (WPP) in this iconic model taxon of sexual selection. In particular, tail streamer length had no detectable association with WPP or a male’s ability to obtain an extra-pair partner. Pairwise comparisons of cuckolded and cuckolding males, involving 76 mixed paternity nests, also supported the hypothesis that male ornamentation does not play a role in determining EPP patterns in the focal barn swallow population. When statistically controlled for clutch initiation date, the probability of obtaining an extra-pair partner only increased with increasing age of males, while WPP was only associated with the age of their female social partners. Our data provide little support for the hypothesis that extra-pair mate choice in our barn swallow population is ornament driven and indicated that age, rather than ornaments, would be a better predictor of paternity.

Background Female promiscuity is highly variable among birds, and particularly among songbirds. Comparative work has identified several patterns of covariation with social, sexual, ecological and life history traits. However, it is unclear whether these patterns reflect causes or consequences of female promiscuity, or if they are byproducts of some unknown evolutionary drivers. Moreover, factors that explain promiscuity at the deep nodes in the phylogenetic tree may be different from those important at the tips, i.e. among closely related species. Here we examine the relationships between female promiscuity and a broad set of predictor variables in a comprehensive data set (N = 202 species) of Passerides songbirds, which is a highly diversified infraorder of the Passeriformes exhibiting significant variation in female promiscuity. Results Female promiscuity was highly variable in all major clades of the Passerides phylogeny and also among closely related species. We found several significant associations with female promiscuity, albeit with fairly small effect sizes (all R2 ≤ 0.08). More promiscuous species had: 1) less male parental care, particularly during the early stages of the nesting cycle (nest building and incubation), 2) more short-term pair bonds, 3) greater degree of sexual dichromatism, primarily because females were drabber, 4) more migratory behaviour, and 5) stronger pre-mating sexual selection. In a multivariate model, however, the effect of sexual selection disappeared, while the other four variables showed additive effects and together explained about 16% of the total variance in female promiscuity. Female promiscuity showed no relationship with body size, life history variation, latitude or cooperative breeding. Conclusions We found that multiple traits were associated with female promiscuity, but these associations were generally weak. Some traits, such as reduced parental care in males and more cryptic plumage in females, might even be responses to, rather than causes of, variation in female promiscuity. Hence, the high variation in female promiscuity among Passerides species remains enigmatic. Female promiscuity seems to be a rapidly evolving trait that often diverges between species with similar ecologies and breeding systems. A future challenge is therefore to understand what drives within-lineage variation in female promiscuity over microevolutionary time scales. Electronic supplementary material The online version of this article (10.1186/s12862-019-1493-1) contains supplementary material, which is available to authorized users.

How males and females contribute to joint reproductive success has been a long-standing question in sexual selection. Under postcopulatory sexual selection (PSS), paternity success is predicted to derive from complex interactions among females engaging in cryptic female choice and males engaging in sperm competition. Such interactions have been identified as potential sources of genetic variation in sexually selected traits but are also expected to inhibit trait diversification. To date, studies of interactions between females and competing males have focused almost exclusively on genotypes and not phenotypic variation in sexually selected traits. Here, we characterize within- and between-sex interactions inDrosophila melanogasterusing isogenic lines with heritable variation in both male and female traits known to influence competitive fertilization. We found surprisingly few genotypic interaction effects on various stages of PSS such as female remating interval, copulation duration, sperm transfer, or sperm storage. Only the timing of female sperm ejection depended on female × male genotypic interactions. By contrast, several reproductive events, including sperm transfer, female sperm ejection and sperm storage, were explained by two- and three-way interactions among sex-specific phenotypes. We also documented complex interactions between the lengths of competing males’ sperm and the female seminal receptacle, which are known to have experienced rapid female-male co-diversification. Our results highlight the non-independence of sperm competition and cryptic female choice and demonstrate that complex interactions between the sexes do not limit the ability of multivariate systems to respond to directional sexual selection.Significance statementFor species with internal fertilization and female promiscuity, postcopulatory sexual selection (PSS) is believed to depend, in part, on complex interactions between rival males and between the sexes. Although little investigated, clarifying such interactions is critical as they may limit the efficacy of PSS in the diversification of reproductive traits (e.g., ejaculate biochemistry and sperm, genitalia and female reproductive tract morphology). Here, we resolve how sex-specific traits and their interactions contribute to key reproductive events and outcomes related to competitive fertilization success, including traits known to have experienced rapid diversification. Our results provide novel insights into the operation and complexity of PSS and demonstrate that the processes of sperm competition and cryptic female choice are not independent selective forces.

The cephalopods (Mollusca: Cephalopoda) are an exceptional class among the invertebrates, characterised by the advanced development of their conditional learning abilities, long-term memories, capacity for rapid colour change and extremely adaptable hydrostatic skeletons. These traits enable cephalopods to occupy diverse marine ecological niches, become successful predators, employ sophisticated predator avoidance behaviours and have complex intraspecific interactions. Where studied, observations of cephalopod mating systems have revealed detailed insights to the life histories and behavioural ecologies of these animals. The reproductive biology of cephalopods is typified by high levels of both male and female promiscuity, alternative mating tactics, long-term sperm storage prior to spawning, and the capacity for intricate visual displays and/or use of a distinct sensory ecology. This review summarises the current understanding of cephalopod reproductive biology, and where investigated, how both pre-copulatory behaviours and post-copulatory fertilisation patterns can influence the processes of sexual selection. Overall, it is concluded that sperm competition and possibly cryptic female choice are likely to be critical determinants of which individuals' alleles get transferred to subsequent generations in cephalopod mating systems. Additionally, it is emphasised that the optimisation of offspring quality and/or fertilisation bias to genetically compatible males are necessary drivers for the proliferation of polyandry observed among cephalopods, and potential methods for testing these hypotheses are proposed within the conclusion of this review. Further gaps within the current knowledge of how sexual selection operates in this group are also highlighted, in the hopes of prompting new directions for research of the distinctive mating systems in this unique lineage.

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa1. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited1,2. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments3,4 in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences5–9. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male–male competition and female choice as discrete processes.

Sperm competition theory has traditionally focused on how male allocation responds to female promiscuity, when males compete to fertilize a single clutch of eggs. Here, we develop a model to ask how female sperm use and storage across consecutive reproductive events affect male ejaculate allocation and patterns of mating and paternity. In our model, sperm use (a single parameter under female control) is the main determinant of sperm competition, which alters the effect of female promiscuity on male success and, ultimately, male reproductive allocation. Our theory reproduces the general pattern predicted by existing theory that increased sperm competition favors increased allocation to ejaculates. However, our model predicts a negative correlation between male ejaculate allocation and female promiscuity, challenging the generality of a prevailing expectation of sperm competition theory. Early models assumed that the energetic costs of precopulatory competition and the level of sperm competition are both determined by female promiscuity, which leads to an assumed covariation between these two processes. By modeling precopulatory costs and sperm competition independently, our theoretical framework allows us to examine how male allocation should respond independently to variation in sperm competition and energetic trade-offs in mating systems that have been overlooked in the past.

Reproductive promiscuity, whereby females are fertilized by extrapair mates, is common. The frequency of extrapair fertilizations (EPFs) depends on at least three sources of variation. First, females may differ in their proneness to being fertilized by extrapair males. Second, males may differ in traits that affect realized promiscuity of females. Third, EPF decisions depend on the combined effects of the identity of social mates. Here, we relied on extensive genetic parentage analysis of the offspring of a socially monogamous bird, the barn swallow, Hirundo rustica, to assess which of the above sources of variation predict the occurrence of EPFs. When we controlled for pair composition and social mate attractiveness, EPFs covaried with morphological and coloration traits of feathers in females. As expected, females mated with highly ornamented, long-tailed males had fewer EPFs. The composition of the breeding pair also accounted for variation in EPFs, implying that the ability of individual males to secure genetic parentage varies between female mates. These results show that females differ in promiscuity, and phenotypic traits of females that are visible to males are associated with promiscuity, potentially serving as cues to prospecting males. Hence, contrary to common interpretations of the negative relationship between male sexual attractiveness and female promiscuity, it can be speculated that larger genetic parentage by highly ornamented males results from their ability to secure the less promiscuous mates rather than from females being less promiscuous when mated to them. Moreover, our study shows that EPFs also depend on the composition of the social pair, as expected if a component of female promiscuity decisions depends on genetic or behavioural compatibility with the social male mate. Our study emphasizes that female promiscuity and its phenotypic correlates, and composition of the social pair, deserve closer attention in studies of sexual selection mediated by EPFs.

Sex is good for us, but it is a compromise. For the benefit of being able to produce genetically variable offspring, we must pay the cost of passing on only half our genes to each of them. Whilst evolutionary biologists still puzzle over the precise details of why the benefits of sex so frequently seem to outweigh the costs (Neiman, Lively, & Meirmans, ), one major challenge to sexual reproduction is the fact that if we pass on only half our genetic material to each gamete, there is a strong incentive for each individual allele to try to gain an unfair representation during gamete production. Fundamental to stabilizing sex once it evolves is therefore the ability to ensure a fair meiosis. Nevertheless, this system is not perfect, and some selfish genetic elements - so-called meiotic drivers - manage to tip the meiotic scales in their favour and gain a transmission advantage (review in Burt and Trivers, ). In this issue of Molecular Ecology, Manser, Lindholm, Simmons, and Firman () demonstrate that in house mice, the effectiveness of one such harmful transmission distorter is reduced by polyandry and hence that population viability can be somewhat restored by female promiscuity.

Although laboratory measurements of whole-animal performance have become a standard tool in evolutionary biology, if and how interindividual variation in performance translates into differential fitness remains poorly understood. Particularly rare are studies that have connected performance to mating and reproductive success in the field. In this study, we use DNA microsatellite parentage analyses to study the fitness gradient in a colour-polymorphic lizard, Podarcis melisellensis. We report on two surprising findings. First, contrary to our expectations, individual sprint speed and bite force capacity correlated negatively, not positively, with male mating and reproductive success. Second, we found an unexpected degree of promiscuity in females. Also, contrary to traditional parental investment theory, the variation in mating success and reproductive success was as high in females as in males. Our results call for a better integration of whole-animal performance and life history traits, and for a reconsideration of the ideas on the likeliness of sexual selection acting on female phenotypes.

Population viscosity can have major consequences for adaptive evolution, in particular for phenotypes involved in social interactions. For example, population viscosity increases the probability of mating with close kin, resulting in selection for mechanisms that circumvent the potential negative consequences of inbreeding. Female promiscuity is often suggested to be one such mechanism. However, whether avoidance of genetically similar partners is a major selective force shaping patterns of promiscuity remains poorly supported by empirical data. Here, we show (i) that fine-scale genetic structure constrains social mate choice in a pair-bonding lizard, resulting in individuals pairing with genetically similar individuals, (ii) that these constraints are circumvented by multiple mating with less related individuals and (iii) that this results in increased heterozygosity of offspring. Despite this, we did not detect any significant effects of heterozygosity on offspring or adult fitness or a strong relationship between pair relatedness and female multiple mating. We discuss these results within the context of incorporating the genetic context dependence of mating strategies into a holistic understanding of mating system evolution.

Female promiscuity can generate postcopulatory competition among males, but it also provides the opportunity for exploitation of rival male ejaculates. For example, in many insect species, male seminal fluid proteins (Sfps) transferred in a female's first mating stimulate increased fecundity and decreased receptivity to remating. Subsequent mates of females could potentially take advantage of the effects of the first male's Sfps and strategically reduce investment in their own ejaculate. We compared postmating responses (fecundity and sexual receptivity) of Drosophila melanogaster females after their first (virgin) matings (V), to the responses of females remating (M) 24 h after their first mating. The results show that M matings fail to boost fecundity and, thus, males are unlikely to gain fitness from transferring Sfps whose sole function—in V matings—is fecundity-stimulation. However, males can protect their likelihood of paternity in M matings through the transfer of receptivity-inhibiting Sfps. The levels of a fecundity-stimulating Sfp (ovulin) were significantly lower in M females relative to V females, at the same time point shortly after the end of mating. In contrast, the levels of a key receptivity-inhibiting Sfp (sex peptide) were the same in M and V females. These results support the hypothesis that males can adaptively tailor the composition of proteins in the ejaculate, allowing a male to take advantage of the fecundity-stimulating effects of the previous male's ovulin, yet maintaining investment in sex peptide. Furthermore, our results demonstrate sophisticated protein-specific ejaculate manipulation.

Science progresses through ideas or hypotheses; novel ways of viewing the world. If those ideas survive testing, then they are considered ‘the truth’, or more crucially, truth-for-now, for the essence of science is that if a new idea provides a better explanation of the way the world is, the truth changes. Darwin’s idea of evolution by natural selection, published as the Origin in 1859, replaced the earlier truth of physico- or natural-theology introduced by John Ray in 1691. Despite resistance by the church, Darwin’s truth gained widespread acceptance, in part due to the efforts of T. H. Huxley, who on reading the Origin said ‘How extremely stupid not to have thought of that!’ Despite natural selection’s enormous explanatory power, there were certain phenomena it apparently could not explain, including female promiscuity. It was only in the 1960s when natural selection was viewed as operating explicitly on individuals (rather than populations or groups), that this changed. Rather than being a cooperative venture between the sexes, sexual reproduction was now viewed in terms of conflicts of interests, and in so doing provided an explanation for female promiscuity (albeit in a male-biased sort of way). Until this point, sexual selection had been concerned exclusively with mate acquisition. With an evolutionary perspective focussing on individuals, it was recognized that sexual selection might continue after insemination, and that rather than competing for partners, males compete for fertilizations. Later it was acknowledged that females, through cryptic processes can also influence the outcome of sperm competition. Today, post-copulatory sexual selection provides explanations for many previously bewildering reproductive traits, including the extraordinary diversity in male and female genitalia, the design of spermatozoa and ova, of seminal fluid and of copulation behaviour itself

Mating systems have a profound influence on the probability of conflict occurring between the sexes. Promiscuity is predicted to generate sexual conflict, thereby driving the evolution of male traits that harm females, whereas monogamy is expected to foster reproductive cooperation, thus rendering such traits redundant. We tested these predictions using experimentally evolved Drosophila pseudoobscura subject to different mating systems. Female survival was not influenced by the mating system treatment of her partner. However, females continuously housed with males evolving under elevated opportunities for female promiscuity produced fewer total progeny, but a relatively greater number of progeny early in their lives, than females housed with males evolving under obligate monogamy. We also found that promiscuous males courted females more frequently than monogamous males. Variation in male courtship frequency and progeny production patterns among treatments reinforces the critical importance of mating system variation for sexual conflict, during both pre- and post-copulatory interactions.

Female promiscuity is common among mammals but its advantages, particularly for marsupials, remain unclear. Using microsatellite DNA from pouch young of known mothers, we identified the most likely fathers of 25 wild spotted-tailed quolls (Dasyurus maculatus) from six litters. We aimed to determine whether young within the same litter had different fathers, and whether breeding success of males was associated with large body mass (consistent with inter-male competition) or scrotal width (consistent with sperm competition). We also explored the possible influence of promiscuity on relatedness within litters. Finally, we used data on paternity and relatedness to make inferences regarding movement and dispersal. Four litters were sired by more than one male, and three males sired offspring in more than one litter. Known fathers had higher body mass, but not scrotal width, than males of unknown paternity status, suggesting that males may compete for access to females. Sires were less related to dams than expected by chance, and litters with multiple paternity had lower relatedness than litters sired by a single male. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 1–7.

SummarySex-ratio distorters are found in numerous species and can reach high frequencies within populations. Here, we address the compelling, but poorly tested, hypothesis that the sex ratio bias caused by such elements profoundly alters their host's mating system. We compare aspects of female and male reproductive biology between island populations of the butterfly Hypolimnas bolina that show varying degrees of female bias, because of a male-killing Wolbachia infection. Contrary to expectation, female bias leads to an increase in female mating frequency, up to a point where male mating capacity becomes limiting. We show that increased female mating frequency can be explained as a facultative response to the depleted male mating resources in female biased populations. In other words, this system is one where male-killing bacteria trigger a vicious circle of increasing male fatigue and female promiscuity.

I analyse and summarize the empirical evidence in mammals supporting alternative benefits that individuals may accrue when committing nonparental infanticide. Nonparental infanticide may provide the perpetrator with nutritional benefits, increased access to limited resources, increased reproductive opportunities, or it may prevent misdirecting parental care to unrelated offspring. The possibility that infanticide is either a neutral or maladaptive behaviour also is considered. I devote the second half of this article to reviewing potential mechanisms that individuals may use to prevent infanticide. These counterstrategies include the early termination of pregnancy, direct aggression by the mother against intruders, the formation of coalitions for group defence, the avoidance of infanticidal conspecifics, female promiscuity, and territoriality. I evaluate the support for each benefit and counterstrategy across different groups of mammals and make suggestions for future research.

Many studies have been aimed at understanding the maintenance of female infidelity in socially monogamous birds. Because engaging in extrapair copulations (EPCs) is believed to be costly for females, it has been argued that EPC behavior must bring indirect benefits to females by elevating offspring fitness. We use empirical data from the literature to assess the relative strength of indirect and direct selection on female EPC behavior, using quantitative genetic approximations of selection. This analysis confirmed that there is generally negative direct selection on EPC behavior caused by depressed paternal investment by social males. In contrast, there was no significant positive indirect selection on EPC behavior in females. A comparison between the two types of selection suggests that the force of direct negative selection is generally much stronger than that of indirect positive selection. Indirect selection is thus unlikely to maintain EPC behavior in the face of direct selection against it. We suggest that EPCs may instead be the result of antagonistic selection on loci influencing the outcome of male-female encounters and that EPC behavior per se may not be adaptive for females but may reflect sexual conflict due to strong selection in males to achieve extrapair copulations.

In most animal species, males are predicted to compete for reproductive opportunities, while females are expected to choose between potential mates. However, when males' rate of reproduction is constrained, or females vary widely in ‘quality’, male mate choice is also predicted to occur. Such conditions exist in the promiscuous mating system of feral Soay sheep on St Kilda, Scotland, where a highly synchronized mating season, intense sperm competition and limitations on sperm production constrain males' potential reproductive rate, and females vary substantially in their ability to produce successful offspring. We show that, consistent with predictions, competitive rams focus their mating activity and siring success towards heavier females with higher inclusive fitness. To our knowledge, this is the first time that male mate choice has been identified and shown to lead to assortative patterns of parentage in a natural mammalian system, and occurs despite fierce male–male competition for mates. An additional consequence of assortative mating in this population is that lighter females experience a series of unstable consorts with less adept rams, and hence are mated by a greater number of males during their oestrus. We have thus also identified a novel male–driven mechanism that generates variation in female promiscuity, which suggests that the high levels of female promiscuity in this system are not part of an daptive female tactic to intensify post–copulatory competition between males.

Postcopulatory sperm competition is a key aspect of sexual selection and is believed to drive the rapid evolution of both reproductive physiology and reproduction-related genes1,2,3,4. It is well-established that mating behavior determines the intensity of sperm competition, with polyandry (i.e., female promiscuity) leading to fiercer sperm competition than monandry1,2,3. Studies in mammals, particularly primates, showed that, owing to greater sperm competition, polyandrous taxa generally have physiological traits that make them better adapted for fertilization than monandrous species, including bigger testes, larger seminal vesicles, higher sperm counts, richer mitochondrial loading in sperm and more prominent semen coagulation2,5,6,7,8. Here, we show that the degree of polyandry can also impact the dynamics of molecular evolution. Specifically, we show that the evolution of SEMG2, the gene encoding semenogelin II, a main structural component of semen coagulum, is accelerated in polyandrous primates relative to monandrous primates. Our study showcases the intimate relationship between sexual selection and the molecular evolution of reproductive genes.

▪ Abstract Extra-pair paternity (EPP) is extremely variable among species of birds, both in its frequency and in the behavioral events that produce it. A flood of field studies and comparative analyses has stimulated an array of novel ideas, but the results are limited in several ways. The prevailing view is that EPP is largely the product of a female strategy. We evaluate what is known about the behavioral events leading to EPP and find the justification for this view to be weak. Conflict theory (derived from selection theory) predicts that adaptations in all the players involved will influence the outcome of mating interactions, producing complex and often highly variable patterns of behavior and levels of EPP. Data support some of these predictions, but alternative hypotheses abound. Tests of predictions from conflict theory will require better information on how males and females encounter one another, behave once they have met, and influence fertilization once insemination has occurred.

Male contests for access to receptive females are thought to have selected for the larger male body size and conspicuous weaponry frequently observed in mammalian species. However, when females copulate with multiple males within an oestrus, male reproductive success is a function of both pre- and postcopulatory strategies. The relative importance of these overt and covert forms of sexual competition has rarely been assessed in wild populations. The Soay sheep mating system is characterized by male contests for mating opportunities and high female promiscuity. We find that greater horn length, body size and good condition each independently influence a male's ability to monopolize receptive females. For males with large horns at least, this behavioural success translates into greater siring success. Consistent with sperm-competition theory, we also find that larger testes are independently associated with both higher copulation rates and increased siring success. This advantage of larger testes emerges, and strengthens, as the number of oestrous females increases, as dominant males can no longer control access to them all. Our results thus provide direct quantitative evidence that male reproductive success in wild populations of mammals is dependent upon the relative magnitude of both overt contest competition and covert sperm competition.

Sperm competition games investigate how males partition limited resources between pre- and post-copulatory competition. Although extensive research has explored how various aspects of mating systems affect this allocation, male allocation between mating, fertilization and parental effort has not previously been considered. Yet, paternal care can be energetically expensive and males are generally predicted to adjust their parental effort in response to expected paternity. Here, we incorporate parental effort into sperm competition games, particularly exploring how the relationship between paternal care and offspring survival affects sperm competition and the relationship between paternity and paternal care. Our results support existing expectations that (i) fertilization effort should increase with female promiscuity and (ii) paternal care should increase with expected paternity. However, our analyses also reveal that the cost of male care can drive the strength of these patterns. When paternal behaviour is energetically costly, increased allocation to parental effort constrains allocation to fertilization effort. As paternal care becomes less costly, the association between paternity and paternal care weakens and may even be absent. By explicitly considering variation in sperm competition and the cost of male care, our model provides an integrative framework for predicting the interaction between paternal care and patterns of paternity.

Gohli et al. (2013) report a positive relationship between genetic diversity and promiscuity across passerine birds, and suggest that female promiscuity acts as a form of balancing selection, maintaining differences in genetic variation across species. This is an interesting hypothesis, but the enormous variation in genetic diversity present within species is not taken into account in their analyses. This, combined with a small sample size at several levels, makes the relationship between genetic diversity and promiscuity very difficult to interpret. Demonstrating that species-level differences in genetic diversity (if they occur at all) are affected by promiscuity would require a far more comprehensive study than is presently possible.

We recently reported a positive association between female promiscuity and genetic diversity across passerine birds, and launched the hypothesis that female promiscuity acts as a balancing selection, pressure maintaining genetic diversity in populations (Gohli et al. 2013). Spurgin (2013) questions both our analyses and interpretations. While we agree that the hypothesis needs more comprehensive empirical testing, we find his specific points of criticism unjustified. In a more general perspective, we call for a more explicit recognition of female mating preferences as mechanisms of selection in population genetics theory.

Passerine birds show large interspecific variation in extrapair paternity rates. There is accumulating evidence that such promiscuous behavior is driven by indirect, genetic benefits to females. Sexual selection theory distinguishes between two types of genetic benefits, additive and nonadditive effects, mediated by preferences for good and compatible genes, respectively. Good genes preferences should imply directional selection and mating skew among males, and thus reduced genetic diversity in the population. In contrast, compatible genes preferences should give balancing selection that retains genetic diversity. Here, we test how well these predictions fit with patterns of variation in genetic diversity and promiscuity levels among passerine birds. We found that more promiscuous species had higher nucleotide diversity at autosomal introns, but not at Z-chromosome introns. We also found that major histocompatibility complex (MHC) class IIB alleles had higher sequence diversity, and therefore should recognize a broader spectrum of pathogens, in more promiscuous species. Our results suggest that female promiscuity targets a multitude of autosomal genes for their nonadditive, compatibility benefits. Also, as immunity genes seem to be of particular importance, we hypothesize that interspecific variation in female promiscuity among passerine birds has arisen in response to the strength of pathogen-mediated selection.

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Explaining the evolution of male care has proved difficult. Recent theory predicts that female promiscuity and sexual selection on males inherently disfavour male care. In sharp contrast to these expectations, male-only care is often found in species with high extra-pair paternity and striking variation in mating success, where current theory predicts female-only care. Using a model that examines the coevolution of male care, female care and female choice; I show that inter-sexual selection can drive the evolution of male care when females are able to bias mating or paternity towards parental males. Surprisingly, female choice for parental males allows male care to evolve despite low relatedness between the male and the offspring in his care. These results imply that predicting how sexual selection affects parental care evolution will require further understanding of why females, in many species, either do not prefer or cannot favour males that provide care.

Humans (Homo sapiens) generally form multiple-male-multiple-female groups that include multiple family units. This social structure is maintained because dominant males do not monopolize females and, thus, allow subordinate males to mate, and human females are not generally promiscuous. Although apes show great variation in mating systems, the human-type mating system is unique among primates. The mating systems of apes and humans have evolved in response to their adaptation to different ecological conditions. We created and analyzed a mathematical model to investigate the conditions for each type of mating system to evolve. We focused on the mating strategy of alpha males and the mating and grouping strategies of females. We defined the human-type mating system as one with multiple-male-multiple-female groups in which alpha males do not monopolize females and females are not promiscuous. We demonstrated that the human-type mating system could evolve when a large group is advantageous and the cost of female promiscuity is great. Moreover, the human- and Pan-type mating systems can be bistable. Our results shed light on the origin of the human family.

Bateman identified two aspects of sexual selection. The first, called Bateman's principle, is that sexual selection favors increased promiscuity of males but not of females as a result of differences in parental investment in gametes. The second is that the variance in mate number of males is the fundamental cause of a sex difference in fitness variance. We argue that Bateman's insight about the source of sexual selection is more fundamental than his speculation about patterns of parental investment. We show that, when the sex ratio is 1:1, the average female must be as promiscuous as the average male, because each copulation involves one male and one female. Because mean male and female promiscuity are tied together in the same manner as mean male and female fitness, a sex difference in mating propensity must be the result of either (1) a sex difference in the covariance between matings and number offspring, or (2) Fisherian run-away sexual selection, wherein female reluctance to mate is a weak form of female choice. We show how female promiscuity can limit the evolution of male promiscuity, turning the central argument of parental investment theory on its head.

Molecular techniques used to assign paternity have revealed previously unknown incidences of extra-pair paternity in socially monogamous bird species. DNA fingerprinting has now been used sufficiently often for mating-system biologists to appreciate the natural variation in the frequency of broods showing extra-pair young. The variation between species and between populations of the same species is surprisingly marked. Explaining this variation may help us to understand the factors promoting sexual selection. Recent comparative studies and detailed behavioural studies suggest that factors such as breeding density, genetic variation in the population and the intensity of sexual conflicts determine the costs and benefits to males and females of engaging in extra-pair copulations, and therefore contribute to the variation among populations.

Female preference genes for large males in the highly promiscuous moth Utetheisa ornatrix (Lepidoptera: Arctiidae) have previously been shown to be mostly Z-linked, in accordance with the hypothesis that ZZ-ZW sex chromosome systems should facilitate Fisherian sexual selection. We determined the heritability of both female and male promiscuity in the highly promiscuous moth U. ornatrix (Lepidoptera: Arctiidae) through parent-offspring and grandparent-offspring regression analyses. Our data show that male promiscuity is not sex-limited and either autosomal or sex-linked whereas female promiscuity is primarily determined by sex-limited, Z-linked genes. These data are consistent with the "sexy-sperm hypothesis," which posits that multiple-mating and sperm competitiveness coevolve through a Fisherian-like process in which female promiscuity is a kind of mate choice in which sperm-competitiveness is the trait favored in males. Such a Fisherian process should also be more potent when female preferences are Z-linked and sex-limited than when autosomal or not limited.

Female promiscuity forces the ejaculates of different males to compete for fertilization through sperm competition. In turn, competing ejaculates often influence female promiscuity and fitness, for example, when ejaculate products increase female fecundity. Here we develop theory examining situations where males stimulate female fecundity and compete for fertilization and female remating is influenced by male fecundity stimulation. We consider the fitness consequences that fecundity stimulation has simultaneously for males inseminating the same female and for the female herself, and we show that the way fecundity increases with male stimulation shifts the coevolutionary dynamics of female remating and male ejaculate expenditure from conflict to cooperation among all mating partners. When fecundity stimulation is weak and males "know" their mating roles, the second male to inseminate a female can exploit the fecundity stimulation of the first male, fostering intra- and intersexual conflict over female remating. However, in a diversity of species where fecundity more than doubles with remating, we show that the female and both males can gain from female remating, leading to intra- and intersexual cooperation over female remating. This coevolutionary perspective yields new insights into the connection between promiscuity, fecundity, and sperm competition and the complex interplay between sexual conflict and cooperation.

Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra- and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm. © 2009 by The National Academy of Sciences of the USA.

Sperm competition theory predicts that males should invest prudently in ejaculates according to levels of female promiscuity. Males may therefore be sensitive to cues in their social environment associated with sexual competition, and tailor investment in sperm production accordingly. We tested this idea experimentally for the first time, to our knowledge, in a mammal by comparing reproductive traits of male house mice ( Mus musculus domesticus ) that had experienced contrasting encounter regimes with potential sexual competitors. We found that daily sperm production and numbers of sperm in the caput epididymis were significantly higher in subjects that had experienced a high encounter rate of social cues from three other males compared to those that had experienced a low encounter rate of social cues from just one other male. Epididymal sperm counts were negatively correlated with the frequency of scent-marking behaviour across all males in our study, suggesting that investment in ejaculate production may be traded off against traits that function in gaining copulations, although there was no difference in overall levels of scent marking between treatment groups. We conclude that social experience-mediated phenotypic plasticity in mammalian spermatogenesis is likely to be adaptive under sperm competition, enabling males to balance the energetic costs and paternity-enhancing benefits of ejaculate production, and is a potentially widespread explanation for intraspecific variation in ejaculate expenditure.

International audience; Based on the sexually selected infanticide (SSI) hypothesis, infanticide can be an adaptive mating strategy for males, but this is has rarely been documented in non-social mammals. This phenomenon should not benefit females, so one would expect females to evolve mating counter strategies in order to protect their infants from infanticidal males. Cases of SSI are extremely difficult to document in the field, especially for non-social species. Using field observations and genetic methods, we describe mating strategies employed by both sexes of brown bears (Ursus arctos) in relation to SSI. We present evidence for the first time suggesting that infanticide is an adaptive male mating strategy in this non-social carnivore, as all requirements for SSI are fulfilled (1) infanticide shortens the time to the mother's next estrus, (2) the perpetrator is not the father of the killed infants, and (3) putative perpetrators sire the next litter. Moreover, all infanticide cases occurred during the mating season. We expected that primarily immigrant males were infanticidal, as in social species. However, we found that resident adult males commonly committed infanticide. Perhaps they recognize females they have mated with previously. Moreover, we used DNA-based parentage testing to demonstrate a minimum of 14.5% of multiple paternities (up to 28% for litters with at least three young). Female promiscuity to confuse paternity may be an adaptive counter strategy to avoid infanticide.

Female promiscuity has broad implications for individual behaviour, population genetics and even speciation. In the field cricket Gryllus bimaculatus, females will mate with almost any male presented to them, despite receiving no recorded direct benefits. Previous studies have shown that female crickets can benefit from polyandry through increased hatching success of their eggs. There is evidence that this effect is driven by the potential of polyandrous females to avoid fertilizing eggs with sperm from genetically incompatible males. We provide direct evidence supporting the hypothesis that polyandry is a mechanism to avoid genetic incompatibilities resulting from inbreeding. Using microsatellite markers we examined patterns of paternity in an experiment where each female mated with both a related and an unrelated male in either order. Overall, unrelated males were more successful in gaining paternity than were related males, but this effect was driven by a much greater success of unrelated males when they were the first to mate.

The relatively small number of ova produced by a female can be fertilized by a single ejaculate in most species. Why females of many species mate with multiple males is therefore enigmatic, especially given that costs associated with remating have been well documented. Recently, it has been argued that females may remate at a maladaptive rate as an outcome of sexually antagonistic coevolution: the evolutionary tug–of–war between manipulation by one sex and resistance to being manipulated by the other sex. We tested this hypothesis experimentally for the evolution of the female remating interval in a naturally promiscuous species, Drosophila melanogaster . In two replicate populations, sexual selection was removed through enforced monogamous mating with random mate assignment, or retained in polyandrous controls. Monogamy constrains the reproductive success of mates to be identical, thereby converting prior conflicts between mates into opportunities for mutualism. Under these experimental conditions, the sexually antagonistic coevolution hypothesis generates explicit predictions regarding the direction of evolutionary change in female remating behaviour. These predictions are contingent upon the mechanism of male manipulation, which may be mediated biochemically by seminal fluids or behaviourally by courtship. Levels of divergence in female remating interval across lines, and in male ejaculatory and courtship effects on female remating, were quantified after 84 generations of selection. Data refute the hypothesis that the evolutionary change in female remating behaviour was due to sexually antagonistic coevolution of courtship signal and receiver traits. The data were, however, consistent with a hypothesis of sexual conflict mediated through ejaculate manipulation. Monogamy–line males evolved ejaculates that were less effective in inducing female non–receptivity and monogamy–line females evolved to remate less frequently, symptomatic of lowered resistance to ejaculate manipulation. The consistency of the results with alternative hypotheses to explain female promiscuity are discussed.

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.