Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

COSTLY INFIDELITY: LOW LIFETIME FITNESS OF EXTRA‐PAIR OFFSPRING IN A PASSERINE BIRD

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.     

Patterns of extra‐pair paternity in mountain chickadees

Extra‐pair paternity (EPP) is common in chickadees and often attributed to the good genes hypothesis. Females generally seek dominant males, who are typically larger, older and sing at higher rates than subordinate males, as extra‐pair sires. In other songbird species, habitat quality and urbanization have been found to influence EPP. Mountain chickadees commonly inhabit suburban habitat, and previous research on our population has shown urbanization may provide benefits to these adaptable songbirds. Here, we ask how individual condition and urbanization influence rates of EPP in mountain chickadees. Over three breeding seasons, we monitored mountain chickadee nests in urban and rural habitat, and determined parentage by genotyping adults and nestlings at six microsatellite loci. Extra‐pair paternity is common in mountain chickadees, with extra‐pair offspring (EPO) in 43.2% of nests and accounting for 17.9% of offspring. We found tenuous support for the good genes hypothesis with females tending to engage in EPCs with older males. However, we did not find an influence of male or female condition on the proportion of EPO in a nest. In addition, we did not find a significant effect of habitat on EPP rates, suggesting the impacts of urbanization on mountain chickadee reproduction may not extend to altering extra‐pair behaviour.     

Age‐dependent changes in infidelity in Seychelles warblers

Extra‐pair paternity (EPP) is often linked to male age in socially monogamous vertebrates; that is, older males are more likely to gain EPP and less likely to be cuckolded. However, whether this occurs because males improve at gaining paternity as they grow older, or because “higher quality” males that live longer are preferred by females, has rarely been tested, despite being central to our understanding of the evolutionary drivers of female infidelity. Moreover, how extra‐pair reproduction changes with age within females has received even less attention. Using 18 years of longitudinal data from an individually marked population of Seychelles warblers (Acrocephalus sechellensis), we found considerable within‐individual changes in extra‐pair reproduction in both sexes: an early‐life increase and a late‐life decline. Furthermore, males were cuckolded less as they aged. Our results indicate that in this species age‐related patterns of extra‐pair reproduction are determined by within‐individual changes with age, rather than differences among individuals in longevity. These results challenge the hypothesis—based on longevity reflecting intrinsic quality—that the association between male age and EPP is due to females seeking high‐quality paternal genes for offspring. Importantly, EPP accounted for up to half of male reproductive success, emphasizing the male fitness benefits of this reproductive strategy. Finally, the occurrence of post‐peak declines in extra‐pair reproduction provides explicit evidence of senescence in infidelity in both males and females.     

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     

Paternal genetic effects on offspring fitness are context dependent within the extrapair mating system of a socially monogamous passerine

Avian extrapair mating systems provide an interesting model to assess the role of genetic benefits in the evolution of female multiple mating behavior, as potentially confounding nongenetic benefits of extrapair mate choice are seen to be of minor importance. Genetic benefit models of extrapair mating behavior predict that females engage in extrapair copulations with males of higher genetic quality compared to their social mates, thereby improving offspring reproductive value. The most straightforward test of such good genes models of extrapair mating implies pairwise comparisons of maternal half-siblings raised in the same environment, which permits direct assessment of paternal genetic effects on offspring traits. But genetic benefits of mate choice may be difficult to detect. Furthermore, the extent of genetic benefits (in terms of increased offspring viability or fecundity) may depend on the environmental context such that the proposed differences between extrapair offspring (EPO) and within-pair offspring (WPO) only appear under comparatively poor environmental conditions. We tested the hypothesis that genetic benefits of female extrapair mate choice are context dependent by analyzing offspring fitness-related traits in the coal tit (Parus ater) in relation to seasonal variation in environmental conditions. Paternal genetic effects on offspring fitness were context dependent, as shown by a significant interaction effect of differential paternal genetic contribution and offspring hatching date. EPO showed a higher local recruitment probability than their maternal half-siblings if born comparatively late in the season (i.e., when overall performance had significantly declined), while WPO performed better early in the season. The same general pattern of context dependence was evident when using the number of grandchildren born to a cuckolding female via her female WPO or EPO progeny as the respective fitness measure. However, we were unable to demonstrate that cuckolding females obtained a general genetic fitness benefit from extrapair fertilizations in terms of offspring viability or fecundity. Thus, another type of benefit could be responsible for maintaining female extrapair mating preferences in the study population. Our results suggest that more than a single selective pressure may have shaped the evolution of female extrapair mating behavior in socially monogamous passerines.     

Multiple hypotheses explain variation in extra‐pair paternity at different levels in a single bird family

Extra‐pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.     

杂色山雀的婚外父权与配偶间的遗传相容性无关

婚配制度作为一种进化稳定对策是动物对某一环境包括种群内部环境适应的结果。据统计,约92%的鸟类为社会性单配制,但单配制鸟类中很多都存在婚外父权现象,表现出社会性婚配制度与遗传性婚配制度的不一致性。杂色山雀(Parus varius)是一种社会性单配制的小型森林洞巢鸟,其是否存在婚外父权现象至今尚未见报道。通过对杂色山雀进行亲权鉴定以确定其有无婚外父权现象及婚外父权的比例,结果显示:45.45%(20/44)的巢存在婚外父权,14.39%(38/264)的后代为婚外子代,说明杂色山雀具有较高的婚外父权水平。进一步探究其婚外父权的发生原因,结果如下:(1)有、无婚外父权巢的社会性亲本之间的遗传相似性无显著差异(P=0.504);(2)有婚外父权巢中婚内子代和无婚外父权巢中子代的杂合度(P=0.118)以及有婚外父权巢中婚外子代与婚内子代的杂合度(P=0.206)均无显著差异。(3)有婚外父权巢中的婚内子代与婚外子代间8项体征指标比较,差异均不显著(Ps0.05)。综上,社会性单配制杂色山雀婚外父权的发生与配偶间的遗传相容性无关,还有待从其他角度进行探究。     

Extra‐pair paternity as a strategy to reduce the costs of heterospecific reproduction? Insights from the crow hybrid zone

Within hybrid zones of socially monogamous species, the number of mating opportunities with a conspecific can be limited. As a consequence, individuals may mate with a heterospecific (social) partner despite possible fitness costs to their hybrid offspring. Extra‐pair copulations with a conspecific may thus arise as a possible post hoc strategy to reduce the costs of hybridization. We here assessed the rate of extra‐pair paternity in the hybrid zone between all‐black carrion crows (Corvus (corone) corone) and grey hooded crows (C. (c.) cornix) and tested whether extra‐pair paternity (EPP) was more likely in broods where parents differed in plumage colour. The proportion of broods with at least one extra‐pair offspring and the proportion of extra‐pair offspring were low overall (6.98% and 2.90%, respectively) with no evidence of hybrid broods having higher EPP rates than purebred nests.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.     

A Contrast in Extra-Pair Paternity Levels on Mainland and Island Populations of Mediterranean Blue Tits

Extra‐pair copulation (EPC) is a widespread behaviour amongst birds, yet the rate of occurrence of extra‐pair offspring is highly variable both within and across species. Two populations of Mediterranean blue tits, Parus caeruleus, one on the mainland and the other on the island of Corsica, are characterized by high levels of extra‐pair paternity (EPP), with 14 and 25% of extra‐pair offspring (in 46 and 68% of the nests), respectively. The rate of EPP is significantly higher in the island population. Such high rates on Corsica contradict the predictions of higher mate fidelity and lower levels of EPP on islands. Despite expressing several traits that characterize an insular syndrome, blue tits of Corsica do not exhibit lower genetic variation which could be associated with low levels of EPP on islands. Furthermore, our results do not support any of the hypotheses that have been proposed so far to explain variation in EPP rates at the local level. We tentatively suggest that proximate Mediterranean constraints, especially consistent food shortage, prompt females to seek better breeding opportunities through a two‐step process including high rates of EPC and divorce.     

Increased extra‐pair paternity in broods of aging males and enhanced recruitment of extra‐pair young in a migratory bird

Despite keen interest in extra‐pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi‐year dataset to test whether traits of a female's social mate influence her propensity to produce extra‐pair offspring in a population of house wrens, and whether producing extra‐pair young has consequences for a female's fitness through effects on offspring survival. Females were most likely to produce extra‐pair offspring when paired with old males and when paired with males on poor‐quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within‐pair young decreased as the age of their sires increased, but cutaneous immunity of extra‐pair young was not affected by the age of their extra‐pair sires or by the age of the males rearing them. Extra‐pair offspring were more likely than within‐pair offspring to return as breeding adults to the local population, with extra‐pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra‐pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.     

Territory configuration moderates the frequency of extra‐group mating in superb fairy‐wrens

The frequency of extra‐pair paternity (EPP) in socially monogamous birds varies substantially between and within species, but ecological drivers of this variation remain poorly understood. Habitat configuration could influence EPP by moderating access to extra‐pair mates, because species occupying territories in a clustered ‘honeycomb’ configuration have a larger pool of potential extra‐group mates in their immediate neighbourhood than those living in linearly arranged territories (e.g. along narrow strips of riparian or fragmented habitat). We exploited variation in the spatial arrangement of territories due to anthropogenic modification of habitat of the cooperatively breeding superb fairy‐wren Malurus cyaneus to test whether habitat configuration influenced the frequency of EPP. In this species, most paternity is obtained by males outside the social group [extra‐group paternity (EGP)]. We found that the frequency of EGP among groups living in linear strips of roadside vegetation (41% of 44 offspring) was lower than it was for groups living in clustered territories within continuous habitat (59% of 70 offspring). Differences in group size and pair relatedness did not explain differences in EGP associated with territory configuration, although the frequency of EGP was negatively correlated with pair relatedness. Our finding suggests that territory configuration can influence rates of EGP and that anthropogenic habitat fragmentation has the potential to limit access to extra‐pair mates, affecting mating systems and ultimately fitness.     

MHC‐dependent survival in a wild population: evidence for hidden genetic benefits gained through extra‐pair fertilizations

Females should prefer to be fertilized by males that increase the genetic quality of their offspring. In vertebrates, genes of the major histocompatibility complex (MHC) play a key role in the acquired immune response and have been shown to affect mating preferences. They are therefore important candidates for the link between mate choice and indirect genetic benefits. Higher MHC diversity may be advantageous because this allows a wider range of pathogens to be detected and combated. Furthermore, individuals harbouring rare MHC alleles might better resist pathogen variants that have evolved to evade common MHC alleles. In the Seychelles warbler, females paired with low MHC‐diversity males elevate the MHC diversity of their offspring to levels comparable to the population mean by gaining extra‐pair fertilizations. Here, we investigate whether increased MHC diversity results in higher life expectancy and whether there are any additional benefits of extra‐pair fertilizations. Our 10‐year study found a positive association between MHC diversity and juvenile survival, but no additional survival advantage of extra‐pair fertilizations. In addition, offspring with a specific allele (Ase‐ua4) had a fivefold longer life expectancy than offspring without this allele. Consequently, the interacting effects of sexual selection and pathogen‐mediated viability selection appear to be important for maintaining MHC variation in the Seychelles warbler. Our study supports the prediction that MHC‐dependent extra‐pair fertilizations result in genetic benefits for offspring in natural populations. However, such genetic benefits might be hidden and not necessarily apparent in the widely used fitness comparison of extra‐ and within‐pair offspring.     

High fidelity: extra‐pair fertilisations in eight Charadrius plover species are not associated with parental relatedness or social mating system

Extra‐pair paternity is a common reproductive strategy in many bird species. However, it remains unclear why extra‐pair paternity occurs and why it varies among species and populations. Plovers (Charadrius spp.) exhibit considerable variation in reproductive behaviour and ecology, making them excellent models to investigate the evolution of social and genetic mating systems. We investigated inter‐ and intra‐specific patterns of extra‐pair parentage and evaluated three major hypotheses explaining extra‐pair paternity using a comparative approach based on the microsatellite genotypes of 2049 individuals from 510 plover families sampled from twelve populations that constituted eight species. Extra‐pair paternity rates were very low (0 to 4.1% of chicks per population). No evidence was found in support of the sexual conflict or genetic compatibility hypotheses, and there was no seasonal pattern of extra‐pair paternity (EPP). The low prevalence of EPP is consistent with a number of alternative hypotheses, including the parental investment hypothesis, which suggests that high contribution to care by males restricts female plovers from engaging in extra‐pair copulations. Further studies are needed to critically test the importance of this hypothesis for mate choice in plovers.     

Genetic diversity does not explain variation in extra‐pair paternity in multiple populations of a songbird

Many songbirds are socially monogamous but genetically polyandrous, mating with individuals outside their pair bonds. Extra‐pair paternity (EPP) varies within and across species, but reasons for this variation remain unclear. One possible source of variation is population genetic diversity, which has been shown in interspecific meta‐analyses to correlate with EPP but which has limited support from intraspecific tests. Using eight populations of the genetically polyandrous red‐winged blackbird (Agelaius phoeniceus), including an island population, we investigated whether population‐level differences in genetic diversity led to differences in EPP. We first measured genetic diversity over 10 microsatellite loci and found, as predicted, low genetic diversity in the island population. Additional structure analyses with multilocus genotypes and mtDNA showed the island population to be distinct from the continental populations. However, the island population's EPP rate fell in the middle of the continental populations' distribution, whereas the continental populations themselves showed significant variation in EPP. This result suggests that genetic diversity by itself is not a predictor of EPP rate. We discuss reasons for the departure from previous results, including hypotheses for EPP that do not solely implicate female‐driven behaviour.     

Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine

Whether female birds choose extra-pair mating partners to obtain genetic fitness benefits is intensely debated. The most straightforward and crucial test of 'good genes' models of female extra-pair mating is the comparison of naturally 'cross-fostered' maternal half-siblings sharing the same rearing environment as any systematic differences in performance between the two categories of offspring phenotype can be attributed to differential paternal genetic contribution. We analysed local recruitment and first-year reproductive performance of maternal half-siblings in the coal tit (Parus ater), a passerine bird with high levels of extra-pair paternity. We provide a highly comprehensive measure of the long-term fitness consequences of female extra-pair matings based on a large sample of 736 within-pair offspring (WPO) and 368 extra-pair offspring (EPO) from 91 first and 55 second broods, from which 132 breeders recruited into the study population. In contrast to predictions derived from 'good genes' models, we found no differences in local recruitment and seven parameters of first-year reproductive performance when comparing WPO and EPO. These results question the universal validity of findings in other bird species supporting 'good genes' models, particularly as they are based on the best approximation to female fitness obtained so far.     

Indirect selection on female extra-pair reproduction? Comparing the additive genetic value of maternal half-sib extra-pair and within-pair offspring

One specific hypothesis explaining the evolution of extra-pair reproduction (EPR) by socially monogamous females is that EPR is under indirect selection because extra-pair offspring (EPO) sired by extra-pair males have higher additive genetic value for fitness than the within-pair offspring (WPO) a female would have produced had she solely mated with her socially paired male. This hypothesis has not been explicitly tested by comparing additive genetic value between EPO and the WPO they replaced. We show that the difference in additive genetic breeding value (BV) between EPO and the WPO they replaced is proportional to the genetic covariance between offspring fitness and male net paternity gain through EPR, and estimate this covariance with respect to offspring recruitment in free-living song sparrows (Melospiza melodia). Recruitment and net paternity gain showed non-zero additive genetic variance and heritability, and negative genetic covariance. Opposite to prediction, EPO therefore had lower BV for recruitment than the WPO they replaced. We thereby demonstrate an explicit quantitative genetic approach to testing the hypothesis that EPR allows polyandrous females to increase offspring additive genetic value, and suggest that there may be weak indirect selection against female EPR through reduced additive genetic value for recruitment of EPO versus WPO in song sparrows.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.