Extra-pair Mating Behaviour Research Articles

Social network position predicts male mating success in a small passerine.

Individuals differ in the quantity and quality of their associations with conspecifics. The resulting variation in the positions that individuals occupy within their social environment can affect several aspects of life history, including reproduction. While research increasingly shows how social factors can predict dyadic mating patterns (who will breed with whom), much less is known about how an individual’s social position affects its overall likelihood to acquire mating partner(s). We studied social networks of socially monogamous blue tits (Cyanistes caeruleus) to investigate whether the number and strength of connections to opposite-sex conspecifics, the ratio between same- and opposite-sex connections, and the tendency to move between social groups in the months prior to breeding affect individuals’ success in acquiring 1) a breeding partner and 2) an extrapair partner. After controlling for differences in spatial location, we show that males that moved more often between social groups were more likely to acquire a breeding partner. Moreover, adult males that associated with more females were more likely to sire extrapair young. The number of female associates also predicted the proportion of familiar female breeding neighbors, suggesting that familiarity among neighbors may facilitate opportunities for extrapair matings. In females, none of the network metrics significantly predicted the likelihood of acquiring a breeding or extrapair partner. Our study suggests that the positioning of males within their social environment prior to breeding can translate into future mating success, adding an important new dimension to studies of (extrapair) mating behavior.

Heritability of the extra-pair mating behaviour of the pied flycatcher in Western Siberia.

Males and females take part in extra-pair copulations in most socially monogamous bird species. The mechanisms leading to the frequent occurrence of extra-pair offspring in socially monogamous couples are strongly debated and unresolved, and they are often difficult to distinguish from one another. Most hypotheses explaining the evolution of extra-pair reproduction suggest selective and adaptive scenarios for their origination and persistence. Is extra-pair paternity a heritable trait? We evaluated the heritability of extra-pair paternity in the pied flycatcher (Ficedula hypoleuca) nesting in Western Siberia. Estimated heritability was low: depending on the model used, the point estimate of the heritability (mode) varied from 0.005 to 0.11, and the bounds of the 95% confidence interval are [0–0.16] in the widest range. Thus, it seems that extra-pair mating behaviour in the pied flycatchers is a plastic phenotypic mating tactic with a small or no genetic component. Our data can help to understand the evolution of extra-pair mating behaviour in socially monogamous species.

Male age is associated with extra-pair paternity, but not with extra-pair mating behaviour

Extra-pair paternity is the result of copulation between a female and a male other than her social partner. In socially monogamous birds, old males are most likely to sire extra-pair offspring. The male manipulation and female choice hypotheses predict that age-specific male mating behaviour could explain this old-over-young male advantage. These hypotheses have been difficult to test because copulations and the individuals involved are hard to observe. Here, we studied the mating behaviour and pairing contexts of captive house sparrows, Passer domesticus. Our set-up mimicked the complex social environment experienced by wild house sparrows. We found that middle-aged males, which would be considered old in natural populations, gained most extra-pair paternity. However, both, female solicitation behaviour and subsequent extra-pair matings were not associated with male age. Further, copulations were more likely when solicited by females than when initiated by males (i.e. unsolicited copulations). Male initiated within-pair copulations were more common than male initiated extra-pair copulations. To conclude, our results did not support either hypothesis regarding age-specific male mating behaviour. Instead, female choice, independent of male age, governed copulation success, especially in an extra-pair context. Post-copulatory mechanisms might determine why older males sire more extra-pair offspring.

Linking the fine-scale social environment to mating decisions: a future direction for the study of extra-pair paternity.

Variation in extra-pair paternity (EPP) among individuals of the same population could result from stochastic demography or from individual differences in mating strategies. Although the adaptive value of EPP has been widely studied, much less is known about the characteristics of the social environment that drive the observed patterns of EPP. Here, we demonstrate how concepts and well-developed tools for the study of social behaviour (such as social network analysis) can enhance the study of extra-pair mating decisions (focussing in particular on avian mating systems). We present several hypotheses that describe how characteristics of the social environment in which individuals are embedded might influence the levels of EPP in a socially monogamous population. We use a multi-level social approach (Hinde, 1976) to achieve a detailed description of the social structure and social dynamics of individuals in a group. We propose that the pair-bond, the direct (local) social environment and the indirect (extended) social environment, can contribute in different ways to the variation observed in the patterns of EPP, at both the individual and the population level. A strength of this approach is that it integrates into the analysis (indirect) interactions with all potential mates in a population, thus extending the current framework to study extra-pair mating behaviour. We also encourage the application of social network methods such as temporal dynamic analysis to depict temporal changes in the patterns of interactions among individuals in a group, and to study how this affects mating behaviour. We argue that this new framework will contribute to a better understanding of the proximate mechanisms that drive variation in EPP within populations in socially monogamous species, and might ultimately provide insights into the evolution and maintenance of mating systems.

Affairs happen-to whom? A study on extrapair paternity in common nightingales.

Most birds engage in extrapair copulations despite great differences across and within species. Besides cost and benefit considerations of the two sex environmental factors have been found to alter mating strategies within or between populations and/or over time. For socially monogamous species, the main advantage that females might gain from mating with multiple males is probably increasing their offspring’s genetic fitness. Since male (genetic) quality is mostly not directly measurable for female birds, (extrapair) mate choice is based on male secondary traits. In passerines male song is such a sexual ornament indicating male phenotypic and/or genetic quality and song repertoires seem to affect female mate choice in a number of species. Yet their role in extrapair mating behavior is not well understood. In this study, we investigated the proportion of extrapair paternity (EPP) in a population of common nightingales Luscinia megarhynchos. We found that EPP rate was rather high (21.5% of all offspring tested) for a species without sexual dimorphism and high levels of paternal care. Furthermore, the occurrence of EPP was strongly related to the spatial distribution of male territories with males settling in densely occupied areas having higher proportions of extrapair young within their own brood. Also, song repertoire size affected EPP: here larger repertoires of social mates were negatively related to the probability of being cuckolded. When directly comparing repertoires sizes of social and extrapair mates, extrapair mates tended to have larger repertoires. We finally discuss our results as a hint for a flexible mating strategy in nightingales where several factors—including ecological as well as male song features—need to be considered when studying reproductive behavior in monogamous species with complex song.

Experimental evidence that brighter males sire more extra-pair young in tree swallows.

Across taxa, extra-pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra-pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra-pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra-pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra-pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra-pair young, and in paired comparisons, extra-pair sires had brighter blue plumage than the within-pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra-pair mating behaviour is driven by benefits to both males and females.

Spatiotemporal and genetic contingency of extrapair behaviour in a songbird

Multiple mating to obtain genetic benefits has been championed as the most likely cause of the evolution of polygamy. However, this assumption has been put into question by an increasing number of recent studies, most of which highlight the importance of considering ecological constraints to comprehend variation in extrapair (EP) behaviour. Here, we studied patterns of extrapair paternity (EPP) in the great tit, Parus major, using data from 11 nestbox plots that differed in population size and breeding conditions. Specifically, we analysed EPP rates in relation to socioecological variables that could influence the way individuals encountered one another in space and time, we tested whether adults engaged in EPP with more heterozygous, more compatible or phenotypically superior individuals than their social mates and we analysed whether extrapair offspring (EPO) were phenotypically or genetically superior to within-pair offspring. Our results do not provide support for the genetic benefit hypothesis from either the male or the female perspective. EPO were heavier than their within-pair paternal half-siblings, but there was no significant difference between EPO and their within-pair maternal half-siblings in terms of phenotypic quality. Regarding socioecological factors, we found a negative relationship between breeding synchrony and EPP rates both within and among plots, which suggests that males face a trade-off between mate guarding and obtaining EPP elsewhere. Our results show that most males engaged in EPP after the fertile period of their social female despite having to travel long distances: about half of the detected cases of EPP involved individuals from different woodlands. This study indicates that when and where to engage in EPP seem to be more relevant factors than with whom to do it and highlights the importance of considering spatiotemporal constraints at a landscape scale to achieve a better understanding of variation in EP mating behaviour.

Are extra-pair males different from cuckolded males? A case study and a meta-analytic examination.

Traditional models for female extra-pair matings assume that females benefit indirectly from extra-pair mating behaviour. Under these so-called adaptive models, extra-pair males are hypothesized to have more compatible genotypes, larger body size, exaggerated ornaments or to be older than cuckolded males. Alternatively, ('nonadaptive') models that consider female extra-pair matings to be a by-product posit that female extra-pair mating can be maintained even if there is no benefit to females. This could happen if, for example, males gained fitness benefits from extra-pair mating, while female and male extra-pair mating behaviours were genetically correlated. Extra-pair males are also expected to be older and larger if this improves their ability to convince or coerce females to mate. We investigated whether a female's extra-pair mates differed from her cuckolded mate in both genetic and phenotypic traits by analysing data from an insular house sparrow population. We found that extra-pair males were older than cuckolded males, consistent with both models. However, in contrast to the expectations from from adaptive models, extra-pair and cuckolded males were of similar genetic relatedness, and hence expected compatibility, with the female, and had comparable body size and secondary sexual traits. We also updated previous meta-analyses examining differences between extra-pair and cuckolded males. The meta-analytic results matched results from our house sparrow case study. Although we cannot completely exclude indirect benefits for females, nonadaptive models may better explain female extra-pair matings. These neglected alternative models deserve more research attention, and this should improve our understanding of the evolution of mating systems.

Malaria infection status predicts extra‐pair paternity in the blue tit

Extra‐pair matings comprise a common reproductive strategy among socially monogamous bird species. However, it remains unclear why females decide to mate with extra‐pair males. Indirect benefits in terms of improving offspring genetic quality are usually invoked to explain this phenomenon. Parasite resistance genes are often considered as a female target of seeking extra‐pair matings, but the direct test of this hypothesis is generally lacking.Here, we report on a relationship between the status of infection with malaria parasites (Plasmodium and Haemoproteus) and occurrence of extra‐pair paternity in a wild population of the blue tit Cyanistes caeruleus inhabiting Gotland (Sweden). We found that the probability of extra‐pair paternity is significantly related to the infection status of social parents. Infected males showed higher probability of being cuckolded than uninfected ones. However, this was observed only among males mated to uninfected females. Thus, avian malaria may potentially contribute to explanation of extra‐pair mating behaviour.

Parental care, loss of paternity and circulating levels of testosterone and corticosterone in a socially monogamous song bird

IntroductionIn biparental birds testosterone levels of males are typically high during the mating phase and decrease during the parental phase. Testosterone implants may enhance mating behaviors, increase the likelihood of males to engage in extra-pair mating behavior and may reduce paternal care. Thus, sex steroids such as testosterone influence reproductive behaviors. Little is known, however, as to whether the more subtle differences in physiological concentrations of testosterone that occur between individuals are related to differences in paternal care, extra-pair behavior, and genetic paternity between those males. Here, we investigate these relationships in the male black redstart (Phoenicurus ochruros), a socially monogamous songbird with a low breeding synchrony. We used nestling provisioning as a proxy for parental care behavior and genetic paternity loss as a proxy for the efficiency of mate-guarding.ResultsThere was no relationship between nestling provisioning and paternity loss of males. Baseline and gonadotropin releasing hormone (GnRH)-induced levels of testosterone, but not baseline corticosterone, were significantly higher during the mating than during the provisioning phase. Males fed more often when temperatures decreased and fed less when they sang more, but we found no correlation between parental behavior and baseline or GnRH-induced testosterone, and baseline corticosterone – both measured during either the mating or the parental phase. However, males that experienced loss of paternity had lower levels of testosterone during the provisioning phase than males that did not lose paternity. Further, males that lost paternity also expressed higher baseline levels of corticosterone.ConclusionsPhysiological differences in testosterone or baseline corticosterone were not related to differences in parental care, suggesting that the variation of testosterone within a physiological range may not relate to the degree of paternal care in this species. However, the profile of both hormones may indicate quality traits that influence the likelihood of the respective male to lose paternity.

Female Red-backed Fairy-Wrens (Malurus melanocephalus) do not appear to pay a cost for high rates of promiscuity

ABSTRACT. Males of monogamous species are expected to increase their overall fitness by engaging in extrapair copulations, but the fitness implications of this behavior for females are somewhat less clear. Numerous studies have examined the potential benefits of extrapair mating to females, but the costs of extrapair mating, which may be substantial, are less well studied. Quantifying these costs is critical to understanding the evolution of extrapair mating behavior in females. We examined the costs of extrapair paternity to female Red-backed Fairy-wrens (Malurus melanocephalus) using an 8-year data set that allowed us to examine both short-term and long-term costs. The variability of individual extrapair mating behavior in female Red-backed Fairy-wrens allowed us to compare the parental care, fecundity, and apparent survival of faithful and promiscuous females. We found no effect of the presence of extrapair offspring on the rate at which males provisioned broods. We also found that promiscuous and fait...

What is sexual selection and the short herstory of female trait variation

What is sexual selection and the short herstory of female trait variation

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.

Female extrapair mating behavior can evolve via indirect selection on males

In many species that form socially monogamous pair bonds, a considerable proportion of the offspring is sired by extrapair males. This observation has remained a puzzle for evolutionary biologists: although mating outside the pair bond can obviously increase the offspring production of males, the benefits of such behavior to females are less clear, yet females are known to actively solicit extrapair copulations. For more than two decades adaptionist explanations have dominated the discussions, yet remain controversial, and genetic constraint arguments have been dismissed without much consideration. An intriguing but still untested hypothesis states that extrapair mating behavior by females may be affected by the same genetic variants (alleles) as extrapair mating behavior by males, such that the female behavior could evolve through indirect selection on the male behavior. Here we show that in the socially monogamous zebra finch, individual differences in extrapair mating behavior have a hereditary component. Intriguingly, this genetic basis is shared between the sexes, as shown by a strong genetic correlation between male and female measurements of extrapair mating behavior. Hence, positive selection on males to sire extrapair young will lead to increased extrapair mating by females as a correlated evolutionary response. This behavior leads to a fundamentally different view of female extrapair mating: it may exist even if females obtain no net benefit from it, simply because the corresponding alleles were positively selected in the male ancestors.

A review and perspective on context-dependent genetic effects of extra-pair mating in birds

The evolutionary origin and the maintenance of extra-pair mating in birds has been a major field of study in the last decades, but no consensus has been reached on the adaptive significance of this behaviour for female birds. The genetic benefit hypothesis proposes that extra-pair sires provide alleles of superior quality and/or better compatibility compared to the social mate, resulting in offspring of higher reproductive value. One frequently adopted approach to test this idea compares the performance of maternal half-siblings in broods with multiple paternity. However, results from such comparisons are inconsistent. Here I discuss the concept that the magnitude of genetic fitness benefits from extra-pair mating depends on the environmental context. To date, context-dependent genetic effects in maternal half-sibling comparisons have been demonstrated for only five passerine bird species. In none of the studies were the crucial environmental conditions experimentally manipulated, and the potentially confounding effects of differential maternal investment in relation to paternity were also largely not accounted for. A number of high-quality data sets on fitness consequences of extra-pair mating behaviour are available that could be (re-) analysed for context-dependence given that relevant gradients of the environment have been recorded and their use is well justified a priori. Such relevant variation may include, for example, the time of breeding in temperate regions, hatching order, but also offspring sex. Primarily, however, experimental approaches are required that systematically and gradually vary fitness-relevant environmental gradients, such as food availability or parasite abundance, and analyse the resulting differential fitness effects while controlling for differential investment. The context dependency of the genetic effects of extra-pair mating behaviour may offer an opportunity for reconciling conflicting results from different extra-pair paternity studies within and across species. More generally, it could allow a better understanding of under which environmental conditions will selection act to maintain a female mating bias towards extra-pair males with potentially far-reaching implications for the ecology and evolution of mating preferences and the maintenance of genetic variation in (sexually) selected traits.

The impact of extra-pair mating behavior on hybridization and genetic introgression

Hybridization and genetic introgression can be associated with secondary contact between closely related species. Previous models have examined the ecological and demographic conditions leading to hybridization and introgression, but few have examined the role of behavior. Alternative mating behaviors are common throughout the animal kingdom but have rarely been recognized as a potential mechanism for hybridization. We developed an individual-based genetic model to examine the hypothesis that extra-pair copulations (EPCs) can lead to hybridization and genetic introgression even when assortative mating preferences are intact. Our model showed that female choice, whether pre- or post-copulation, reinforced species boundaries and that hybrids were relatively uncommon when no EPCs occurred. However, when EPCs were introduced into the model, the proportion of hybrids in the population depended on the strength of female mate or sperm choice, the strength of male pursuit of EPCs, and habitat-induced effects on the species composition of the neighborhood. As predicted, male pursuit of EPCs caused extensive introgression, but female preference for conspecific paternity reinforced species differences. Inclusion of mitochondrial markers of species identity revealed significant effects of interspecific and intersexual behavior during EPCs on the direction of introgression. These results suggest that an alternative mating tactic may have major effects on the level of genetic homogenization and can cause local extinction of a species.

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet

Within-pair young are more immunocompetent than extrapair young in mixed-paternity broods of the red bishop

Two competing hypotheses are commonly used to explain matings with multiple males in female birds. The genetic benefit model sees extrapair copulations as a means to enhance offspring viability, while the fertility-insurance hypothesis states that females copulate with multiple males to guarantee fertilization of eggs. According to the genetic benefit hypothesis, extrapair young are expected to have a genetic advantage over their maternal half-sibs raised in the same brood. A quantifiable measure for offspring quality is the immunocompetence, the ability of an individual to cope with infections. In this study, we used the phytohaemagglutinin induced skin-swelling response technique to test whether the cell-mediated immune reaction differs between extrapair and within-pair nestlings from mixed-paternity broods in the polygynous red bishop, Euplectes orix. The strength of the nestlings' immune response was positively linked to general health status and immunological condition of their genetic fathers, indicating a heritable component of nestling immunocompetence. We found that extrapair young were actually significantly less immunocompetent than within-pair young from the same nest, a result that does not lend support to the genetic benefit hypothesis. We suggest that female red bishops mated to successful high-quality males engage in extrapair copulations to insure against temporary infertility in their social mates caused by sperm depletion because of frequent copulations with their multiple female partners. This result, however, was significant only in the hotter of 2 years, indicating that environmental factors can obscure variation in nestling fitness arising from female extrapair mating behaviour.

Yearling male great tits, Parus major, suffer more strongly from cuckoldry than older males

In the majority of socially monogamous bird species, females have offspring sired by males other than their social mate as the result of extra-pair copulations. While it is widely recognised that there is considerable variation in the frequency of extra-pair paternity between species, between populations of a species and between individuals of a population, determinants of this variation are surprisingly difficult to establish. With respect to individual variation within a population, it is an important step to test for male and female correlates of cuckoldry to better understand the patterns as well as the adaptive significance of extra-pair mating behaviour. Here, we analysed patterns of extra-pair paternity in relation to male age, female age and their interaction in the great tit Parus major, a socially monogamous passerine with a moderate frequency of extra-pair paternity. Based on a large sample of 316 genotyped first broods from five successive years, we failed to demonstrate interaction effects of male and female age on both the proportion of extra-pair offspring and the likelihood that at least one extra-pair offspring is present within a brood. However, both the proportion of extra-pair offspring and the likelihood of paternity loss were higher for yearling as compared to older males, while this was not the case for yearling vs. older females. Furthermore, the proportion of extra-pair offspring within a brood decreased with increasing age of the attending male in within-individual analyses. We found a comparable effect also for attending females in within-individual analyses, but only when excluding two individuals with 100% extra-pair paternity. A female (extra-pair) mating preference for older males and/or a limited ability of yearling males to prevent cuckoldry in their broods could explain these age-related patterns of paternity loss. Effect sizes, however, were not particularly large and substantial residual variation within age categories suggests the importance of further yet unidentified determinants of variation in paternity loss in the study population.

Male age predicts extrapair and total fertilization success in the socially monogamous coal tit

An important step to a better understanding of the adaptive significance of extrapair mating behavior in socially monogamous species is to uncover the identity of extrapair sires (EPS). Here, we used a combination of multilocus DNA fingerprinting and microsatellite analysis to identify EPS in the socially monogamous coal tit (Periparus ater), a passerine bird with high rates of extrapair paternity. We then analyzed how fertilization success was related to male age in 2 consecutive first brood periods based on knowledge of the exact age of the majority of territorial males. EPS were significantly older compared with the males they cuckolded. Furthermore, extrapair and, as a consequence, also total fertilization success were positively related to male age, while within-pair success was not. Interestingly, fertilization success did not increase linearly with male age but leveled off for older age classes and was most parsimoniously described by the inverse term of male age. Results were consistent over the 2 years, while the demography of the study population differed with respect to the age distribution of territorial males. Furthermore, we also show that individual males increased their extrapair fertilization (EPF) success with age indicating that cross-sectional analyses were not confounded by cohort effects. Together with the results from other species, these findings suggest that male age (or a strong correlate thereof) is a major determinant of EPF success in several socially monogamous bird species.