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The perceived risk of predation can affect breeding behaviour and reduce reproductive success in prey species. Individuals exposed to predators may also adopt different mating tactics with potential consequences for the distribution of paternity in socially monogamous species that engage in extra‐pair copulations. We experimentally increased perceived predation risk during the fertile period in blue tits Cyanistes caeruleus. Every morning between nest completion and the onset of egg laying, we presented a model of either a predator or a non‐predator (control) near active nestboxes. Broods from pairs exposed to predators had higher levels of extra‐pair paternity than control broods. This mainly resulted from a higher proportion of extra‐pair offspring in broods with at least one extra‐pair young. Females exposed to predators first emerged from the nestbox later in the morning, stayed away from the nestbox for longer and were less likely to be visited at the nest by their social mate, but we detected no behavioural differences once the model was removed. Our results suggest that the higher rates of extra‐pair paternity resulted from the disruption of morning routines, which may have inhibited within‐pair copulations or increased opportunities for females to engage in extra‐pair copulations. We conclude that the perceived risk of predation can have substantial effects on levels of extra‐pair paternity. Perceived predation risk can have many behavioural consequences, but how it affects mating behaviour has rarely been tested. The authors exposed blue tits to predator models during the peak fertile period and found that levels of extra‐pair paternity were substantially increased, possibly because early morning behaviour was disrupted.

In socially monogamous species, extra-pair paternity (EPP) is predicted to increase variance in male reproductive success (RS) beyond that resulting from genetic monogamy, thus, increasing the “opportunity for selection” (maximum strength of selection that can act on traits). This prediction is challenging to investigate in wild populations because lifetime reproduction data are often incomplete. Moreover, age-specific variances in reproduction have been rarely quantified. We analyzed 21 years of near-complete social and genetic reproduction data from an insular population of Seychelles warblers (Acrocephalus sechellensis). We quantified EPP’s contribution to lifetime and age-specific opportunities for selection in males. We compared the variance in male genetic RS vs social (“apparent”) RS (RSap) to assess if EPP increased the opportunity for selection over that resulting from genetic monogamy. Despite not causing a statistically significant excess (19 %) of the former over the latter, EPP contributed substantially (27 %) to the variance in lifetime RS, similarly to within-pair paternity (WPP, 39 %) and to the positive WPP-EPP covariance (34 %). Partitioning the opportunity for selection into age-specific (co) variance components, showed that EPP also provided a substantial contribution at most ages, varying with age. Therefore, despite possibly not playing the main role in shaping sexual selection in Seychelles warblers, EPP provided a substantial contribution to the lifetime and age-specific opportunity for selection, which can influence evolutionary processes in age-structured populations.

Biparental care is common in socially monogamous avian species, but both partners may seek extra‐pair copulations (EPCs). The relative costs and benefits of EPCs between the sexes are likely complex, yet the implications of EPCs for parental care behavior have been examined predominantly in males. Not only could females benefit from EPCs, but females would have additional information about the likelihood of extra‐pair young (EPY) in their nest not available to their partners, which likely influences female behavior. We examined how the presence and abundance of EPY in a nest affect parental behavior in a socially monogamous songbird, song sparrows (Melospiza melodia ). We predicted that females who mated outside the social pair would invest more in a clutch with a higher probability of EPY. We monitored nest visitation rates by male and female social partners as a proxy for parental investment and quantified extra‐pair paternity in 45 nests. Maternal visitation rates were higher in nests with EPY compared to nests without, while males did not adjust their investment in relation to the presence of EPY. These findings support our prediction that females who participated in EPC would invest more in the resulting offspring. We explored the relationship between maternal and paternal investment (nest visitation rates) and the paternity of nestlings in a wild, socially monogamous songbird. We found that maternal investment was positively associated with the presence, number, and proportion of extra‐pair nestlings, but there was no relationship between paternal investment and extra‐pair young. These findings support our prediction that females who participated in extra‐pair copulations would invest more in the resulting offspring.

Olfaction can aid individuals in finding genetically compatible mates in many animals, while high levels of mixed paternity may result from a limited ability to evaluate their mate's genetic profile against their own before mating. To test this suggestion and explore if olfaction may indeed influence mating patterns in birds, we combined published measures of olfactory ability with data on genetic mating pattern in the same species, across a phylogenetically broad range of species. We used three measures of olfaction: (1) olfactory bulb diameter, (2) olfactory bulb volume and (3) number of olfactory receptor genes (148, 134 and 48 species, respectively). These measures were then matched to species‐specific estimates of mating pattern, measured as percentage of broods with mixed paternity (> 1 male siring offspring in the same brood). Limited overlaps between the datasets resulted in 30 matched species for olfactory bulb diameter, 31 for olfactory bulb volume and 15 for olfactory receptor genes. Controlling for brain size (telencephalon), we then correlated olfaction to mating pattern, and found that the bigger the relative olfactory bulb diameter, the lower the proportion of mixed paternity. In contrast, there was no significant correlation between olfactory bulb volume or number of receptor genes and paternity. This study thus indicates that mating patterns in birds may be influenced by olfactory ability, measured as olfactory bulb diameter. Next, we suggest expanding the datasets by collecting olfactory‐focused measures, targeting species for which paternity measures already exist, to allow a full phylogenetic analysis. Olfaction can help individuals finding genetically compatible mates in many animals, while high levels of mixed paternity may reflect a reduced ability to evaluate a mate's profile against their own before mating. We tested this hypothesis by matching estimates of olfactory ability with mixed paternity for a broad range of bird species. As predicted, we found that the bigger the relative olfactory bulb diameter, the lower the percentage of broods with mixed paternity. However, we found no correlation between two other measures of olfactory ability and mixed paternity.

Males of socially monogamous species can increase their siring success via within-pair and extra-pair fertilizations. In this study, we focused on the different sources of (co)variation between these siring routes, and asked how each contributes to total siring success. We quantified the fertilization routes to siring success, as well as behaviors that have been hypothesized to affect siring success, over a five-year period for a wild population of great tits Parus major. We considered siring success and its fertilization routes as \"interactive phenotypes\" arising from phenotypic contributions of both members of the social pair. We show that siring success is strongly affected by the fecundity of the social (female) partner. We also demonstrate that a strong positive correlation between extra-pair fertilization success and paternity loss likely constrains the evolution of these two routes. Moreover, we show that more explorative and aggressive males had less extra-pair fertilizations, whereas more explorative females laid larger clutches. This study thus demonstrates that (co)variation in siring routes is caused by multiple factors not necessarily related to characteristics of males. We thereby highlight the importance of acknowledging the multilevel structure of male fertilization routes when studying the evolution of male mating strategies.

In social mammals, dominance status and tenure length are often important determinants of male reproductive success. Nevertheless, alternative strategies, such as extra‐pair mating, and the active role of females in securing reproductive benefits can substantially modify patterns of paternity. To date, many studies have had short observation periods and small sample sizes, constraining understanding of how male social status, tenure length, and female mating strategies jointly affect male long‐term reproductive success, especially in species with complex social systems. Using longitudinal demographic and genetic data from a free‐ranging population of a golden snub‐nosed monkey (Rhinopithecus roxellana) multilevel society in the Qinling Mountains, central China, we investigated how leader males' ranks and tenure lengths influence their reproductive success through within‐unit and extra‐unit paternities. We found that although high rank increases the likelihood of producing within‐unit paternity offspring in the short term, tenure length is a stronger determinant of long‐term reproductive success via both within‐unit and extra‐unit paternities. Females may gain direct benefits from producing extra‐pair paternity offspring by reducing the risk of infanticide through mating with all‐male band males and/or by selecting high‐ranking leader males for better access to resources. Moreover, females may also accrue additional indirect benefits from producing extra‐pair paternity offspring when more adult males are available in the breeding band. Our findings highlight extra‐pair paternity as a reproductive strategy for both male and female golden snub‐nosed monkeys to optimize reproductive success, which may also play a role in maintaining stability in this complex primate society. This paper is the latest study to explore the effects of social status and reproductive strategy intake on the males' long‐term reproductive success in a multilevel society using longitudinal demographic and genetic data. The findings of this study further expand the significance of extra‐pair paternity as a reproductive strategy, revealing how social species balance intersexual conflict in comparative studies of reproductive success.

Social monogamy is the prevalent mating system in birds, but alternative strategies of extra‐pair paternity (EPP) and conspecific brood parasitism (CBP) occur in many species. Raptors are virtually absent in discussions of broad taxonomic reviews regarding EPP and CBP likely because these strategies are mostly absent or at low frequency; CBP is unreported in solitary nesting raptors. In contrast, we found high frequencies of EPP (16%–31%) and CBP (15%–26%) nests among three populations of Cooper's Hawks (Accipiter cooperii) across the northern breeding range of this solitary nesting, socially monogamous species. EPP and CBP combined occurred in 42%–46% of all nests among populations and hence unexpectedly were nearly equivalent to proportions of genetically monogamous nests. Select covariates failed to predict presence of EPP and CBP in part because virtually all extra‐pair adults were uncaught and likely were floaters. We found no support for the hypothesis that territorial females traded copulations for food to maximize energy intake for increased production. Our unique discoveries enhance knowledge of the extent and diversity of alternative breeding strategies among groups of avian and other animal species. Raptors are virtually absent in discussions of broad taxonomic reviews regarding extra‐pair paternity (EPP) and conspecific brood parasitism (CBP) likely because these strategies are mostly absent or at low frequency. In contrast, we found high frequencies of EPP (16%–31%) and CBP (15–26%) per nest among three populations of Cooper's Hawks (Accipiter cooperii) across the northern breeding range of this solitary nesting, socially monogamous species. Our unique discoveries enhance knowledge of the extent and diversity of alternative breeding strategies among groups of avian and other animal species.

Sexually transmitted microbes are hypothesized to influence the evolution of reproductive strategies. Though frequently discussed in this context, our understanding of the reproductive microbiome is quite nascent. Indeed, testing this hypothesis first requires establishing a baseline understanding of the temporal dynamics of the reproductive microbiome and of how individual variation in reproductive behavior and age influence the assembly and maintenance of the reproductive microbiome as a whole. Here, we ask how mating activity, breeding stage, and age influence the reproductive microbiome. We use observational and experimental approaches to explain variation in the cloacal microbiome of free‐living, female tree swallows (Tachycineta bicolor). Using microsatellite‐based parentage analyses, we determined the number of sires per brood (a proxy for female mating activity). We experimentally increased female sexual activity by administering exogenous 17ß‐estradiol. Lastly, we used bacterial 16S rRNA amplicon sequencing to characterize the cloacal microbiome. Neither the number of sires per brood nor the increased sexual activity of females significantly influenced female cloacal microbiome richness or community structure. Female age, however, was positively correlated with cloacal microbiome richness and influenced overall community structure. A hypothesis to explain these patterns is that the effect of sexual activity and the number of mates on variation in the cloacal microbiome manifests over an individual's lifetime. Additionally, we found that cloacal microbiome alpha diversity (Shannon Index, Faith's phylogenetic distance) decreased and community structure shifted between breeding stages. This is one of few studies to document within‐individual changes and age‐related differences in the cloacal microbiome across successive breeding stages. More broadly, our results contribute to our understanding of the role that host life history and behavior play in shaping the cloacal microbiomes of wild birds. In this paper, we ask the question: how do mating activity, breeding stage, and age influence female reproductive microbiomes? We address this question using observational and experimental approaches to explain both between‐ and within‐individual variation in the cloacal microbiome of free‐living, female birds that exhibit differences in extra‐pair paternity rates. We found that female age and breeding stage, but not number of mates or experimentally elevated sexual activity (via 17ß‐estradiol implants), significantly influenced cloacal microbiome alpha diversity and explained variation in bacterial community structure.

Extra-pair copulation (EPC) is widespread in socially monogamous species, but its evolutionary benefits remain controversial. Indirect genetic benefit hypotheses postulate that females engage in EPC to produce higher quality extra-pair offspring (EPO) than within-pair offspring (WPO). In contrast, the sexual conflict hypothesis posits that EPC is beneficial to males but not to females. Thus, under the sexual conflict hypothesis, EPO are predicted to be no fitter than WPO. We tested these two hypotheses in a 12-year dataset with complete life-history and pedigree information from an isolated island population of house sparrows (Passer domesticus). We compared fitness components of EPO and two types of WPO: (1) WPO from genetically polyandrous ″unfaithful″ mothers, and (2) WPO from genetically monogamous mothers. We found that all three groups of offspring had similar probabilities of hatching and nestling survival. Unexpectedly, EPO had the lowest probability of recruiting into the breeding population and the lowest lifetime reproductive output. Our results indicate that EPO incurred indirect genetic costs, rather than benefits, which is contrary to indirect benefit models. Importantly, the indirect costs we observed are also underappreciated in current sexual conflict models. Our results call for improved theoretical frameworks that incorporate indirect costs by extending current sexual conflict models.

Most of what is known about extra-pair paternity in hole-nesting birds derives from studies using artificial nesting sites, such as nestboxes. However, it has rarely been investigated whether inference drawn from breeding events taking place in nestboxes matches what would be observed under natural conditions, that is, in natural cavities. We here report on a variation in promiscuity in blue tits and great tits nesting in natural cavities and nestboxes in an urban forest in Warsaw, Poland. Specifically, we tested whether local breeding density, local breeding synchrony, and extra-pair paternity (inferred from SNP data generated with a high-throughput genotyping by sequencing method) differed between birds nesting in natural cavities and nestboxes. In both blue tits and great tits, the frequency of extra-pair paternity was similar between the two cavity types. In blue tits, we observed shorter nearest neighbor distance, higher neighbor density, and higher synchronous neighbor density (i.e., density of fertile females) in nestboxes relative to natural cavities. No such pattern was found in great tits. Moreover, we detected a positive relationship between the proportion of extra-pair offspring in the nest and neighbor density around the nest in blue tits. Our results revealed that the provisioning of nestboxes did not change rates of extra-pair paternity, suggesting that conclusions drawn from nestbox studies might adequately represent the natural variation in extra-pair matings in some species or sites. However, the observed differences in spatiotemporal components of breeding dynamics highlight the fact that these parameters should be carefully considered when comparing mating behavior across studies and/or sites.