Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males

Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.     

Experimental mate replacement does not increase extra-pair paternity in tree swallows

Before the onset of female fertility, we removed 12 early-settling male tree swallows (Tachycineta bicolor) from their nest-boxes and mates, and allowed replacement males which had been floaters to settle with the original female residents. We predicted that females which had their original mate choice altered (experimentals) would be more likely to obtain extra-pair fertilizations than females which remained paired with their original, early-settling mates (controls). The proportion of females obtaining extra-pair fertilizations, however, did not differ between controls and experimentals, indicating that mating tactics of female tree swallows were unaffected by mate replacement. However, differences between early-settling and replacement males did exist. Replacement males had shorter wing chords than early-settling males, suggesting that they were younger. Moreover, a significantly greater proportion of replacement males than early-settling males were unringed and thus new to the study site. Our results suggest that if females are choosing males for good genes, then early-settling males are not superior in genetic quality to the smaller replacement males which had originally been floaters.     

Genetic and behavioural evidence of monogamy in a mammal,Kirk's dik-dik (Madoqua kirkii).

Little is known about the mating behaviour of monogamous mammals. Here, we present behavioural and genetic evidence of fidelity in a socially monogamous dwarf antelope, Kirk''s dik-dik. DNA microsatellite analysis revealed no evidence of extra-pair paternity (EPP) in dik-diks: mothers'' partners matched the paternal genotype in all 12 juveniles tested. One likely reason for the absence of EPP is that males guard their mates closely during oestrus and over-mark all female scent, thereby reducing the likelihood of other males attempting to mate. In addition, males may be limited in their ability to search for extra-pair populations (EPCs) by activities associated with pair-bond maintenance. Year-round, males maintained proximity within pairs, followed their females'' activity patterns, and spent approximately 64% of their time with their partners. However, males did attempt to obtain EPCs when the opportunity arose, and genetic monogamy in dik-diks is probably best explained by the behaviour of females: in contrast to many monogamous female birds, female dik-diks do not appear to seek EPC partners. We propose that females avoid extra-pair males because they are unable to mate with them without instigating a potentially dangerous conflict.     

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.     

Low frequency of extra-pair fertilisations in House Sparrows breeding at high density

The importance that the density of breeders has on the opportunity for extra-pair fertilisations (EPFs) is controversial. Some evidence supports the idea that population density and frequency of extra-pair paternity are positively associated, whereas other work does not. In the present paper we estimate EPF frequency in a dense House Sparrow Passer domesticus colony. We detected extra-pair nestlings in 9.3% of 54 broods studied, and 7% of 171 nestlings were sired by extra-pair fathers. The number of clutches laid per female, the change of male or female between two consecutive breeding attempts and the age of the partners showed no association with the presence or absence of extra-pair fertilisations. Morphometric variables of paired males and females did not discriminate broods with EPFs from those without. We detected a single case of a female laying a "parasitic" egg in the nest of a male that in a previous breeding attempt was the extra-pair genetic father of her entire brood. The frequency of extra-pair fertilisation recorded in this study was low compared with that in other House Sparrow populations breeding at lower densities, or other species that breed in colonies. This result does not support the claim that EPF frequency is associated with population density. We propose, as an explanation for this result, that under high intra-sexual competition for nest sites (1) males may have limited opportunities to search for females for extra-pair copulations and (2) the high quality of male nest-owners may reduce female propensity to search for additional sexual partners.     

Tests of spatial and temporal factors influencing extra-pair paternity in red-winged blackbirds

Extra-pair paternity (EPP) is a widespread and highly variable reproductive phenomenon in birds. We tested the effects of habitat, spatial factors, and timing of breeding on the occurrence of EPP in red-winged blackbirds (Agelaius phoeniceus). We used PCR-amplified microsatellites to assess the paternity of 1479 nestlings from 537 broods on 235 territories over four breeding seasons. Over 4 years, 40% of nestlings were extra-pair. At least 27% of actual sires were non-neighbours, suggesting that males or females interacted over longer distances than in other populations of red-winged blackbirds. The level of EPP was significantly clumped within broods and males but not within females across broods. EPP was negatively related to the area of a male's territory. The spatial proximity of a female's nest to the territory boundary had no effect on total EPP, but tended to increase the probability of an EPP by a nearby male. We found no influence on EPP of the type of habitat on the territory or the level of nesting activity nearby. The time in the season when a nest was started and the synchrony of breeding also had no significant effect on the level of EPP. The age of the male, the age of his neighbours, and the interaction between the two had no effect on total EPP. However, older males were less likely to have an offspring sired by a neighbour on their territory. Males with older neighbours were also less likely to have offspring sired by a neighbour, particularly if they were new territory owners. The high variability in who gained and lost paternity, and the limited impact of spatial and temporal factors influencing it, have some interesting implications for theories seeking to explain mating patterns.     

大山雀的婚外父权调查

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,在动物生殖过程中具有重要意义.大山雀(Parus major)是一种广域分布物种,研究显示广域分布物种的形态、生理、行为、生态特征及婚配制度在不同地区或种群间存在显著差异,因此,该文选择了分布于中国辽宁仙人洞国家级自然保护区的大山雀(P.m.minor)种群开展其婚配制度研究.野外共采集了22巢大山雀亲代和子代血液样本.结果如下:(1)从11个微卫星位点中筛选出了8个多态性较好的微卫星位点用于大山雀父权鉴定,在母本已知的情况下确定父权的准确率可达99.98％;(2)巢内父权鉴定结果显示,31.8％ (7/22)的巢包含婚外父权,8.12％ (16/197)的子代为婚外子代.与其他森林雀形目鸟类相比,大山雀婚外子代的比例明显偏低(＜10％),每个存在婚外父权巢的婚外子代比例各异(55.6％～9.1％),且无明显规律.     

Extra-pair paternity does not result in differential sexual selection in the mutually ornamented black swan (Cygnus atratus)

We studied patterns of parentage in 85 broods (332 cygnets) of black swans during three breeding seasons, using a set of eight polymorphic microsatellite markers. We detected both intraspecific brood parasitism (IBP; < 5% of cygnets per year) and extra-pair paternity (EPP). In these years, 10-17% (mean = 15.1%) of cygnets resulted from EPP, and 27-40% (mean 37.6%) of broods contained at least one extra-pair cygnet. Compared with levels of EPP in closely related species with similar life histories, these values are unexpectedly high. EPP in black swans appears unrelated to ecological factors (breeding density and synchrony) or genetic factors (genetic similarity between pair members or genetic quality of the offspring). We found no evidence that a mutual sexual feather ornament known to play a role in social mate choice in black swans (curled wing feathers) is involved in extra-pair mate choice. EPP does not lead to greater variance in reproductive success in males, relative to females in this species. We therefore suggest that EPP does not result in differential sexual selection on males and females, explaining why they are ornamented to the same degree.     

Age trajectories in extra-pair siring success suggest an effect of maturation or early-life experience

Across birds, male age is the most consistent predictor of extra-pair siring success, yet little is known about age effects on paternity over the lifetime of individuals. Here, we use data from a 13-year study of a population of blue tits (Cyanistes caeruleus) to investigate how extra-pair siring success changes with age within individuals. Our results indicate that extra-pair siring success does not continuously increase with male age. Instead, siring success was related to male age in a threshold fashion, whereby yearling males were less likely to gain paternity than older males. This effect was independent of the age of the social partner, but influenced by the age of the extra-pair female: success of yearlings at siring extra-pair young (EPY) with older females was even lower. Among males that sired at least one EPY, the number of extra-pair mates and the proportion of EPY sired were unrelated to male age. We found no evidence for an influence of selective disappearance on extra-pair reproduction. Senescence, if anything, only occurs at ages blue tits rarely reach. A literature review indicates that an effect of male age on extra-pair siring success may be limited to the switch from yearling to older in many species. Thus, the generally observed age effect on male extra-pair siring success may be linked to age class rather than continuous ageing. This suggests that lack of experience or not fully completed maturation are important drivers of age patterns in extra-pair paternity.     

High frequency of extra‐pair paternity in an urban population of Cooper's Hawks

Raptors exhibit some of the highest rates of intra‐pair copulations among birds, perhaps in an attempt by males to reduce the risk of being cuckolded. Indeed, the frequency of extra‐pair fertilizations reported in studies of raptors to date is relatively low (0–11.2%). Socially monogamous Cooper's Hawks (Accipiter cooperii) exhibit one of the highest copulation rates among birds, yet there are no published accounts of extra‐pair copulations (or paternity). We studied a population of Cooper's Hawks in Milwaukee, Wisconsin, during three breeding seasons (2003, 2004, and 2007), examining the possible effects of age (1 yr old vs. ≥ 2 yr old), adult mass, and brood size on the frequency of extra‐pair paternity (EPP). We found that 19.3% of nestlings (N = 27/140) were extra‐pair young (EPY), and 34% of all broods (N = 15/44) had at least one EPY. The sires of the EPY in our study were identified for only two broods, suggesting that floater males may have engaged in extra‐pair copulations with territorial females. We found that brood size was a good predictor of the occurrence of EPP (EPP) in nests, but adult mass and female age were not. To our knowledge, these possible correlates of the occurrence of EPP in raptors had not previously been investigated. Male Cooper's Hawks provide food for females during the pre‐nesting period, and delivery of food is, in contrast to other raptor species, typically followed by copulation. Thus, one possible explanation of the relatively high rates of EPP in our study is that females might accept or even solicit extra‐pair copulations from males other than their mates as a means of maximizing energy intake for egg production. Such behavior might be particularly likely in our study area, i.e., a food‐rich urban setting with a high breeding density of Cooper's Hawks.     

Social common mole-rats enhance outbreeding via extra-pair mating

Females in many species engage in matings with males that are not their social mates. These matings are predicted to increase offspring heterozygosity and fitness, and thereby prevent the deleterious effects of inbreeding. We tested this hypothesis in a cooperative breeding mammal, the common mole-rat Cryptomys hottentotus hottentotus. Laboratory-based studies suggested a system of strict social monogamy, while recent molecular studies indicate extensive extra-pair paternity despite colonies being founded by an outbred pair. Our data show that extra-pair and within-colony breeding males differed significantly in relatedness to breeding females, suggesting that females may gain genetic benefits from breeding with non-resident males. Extra-colony male mating success was not based on heterozygosity criteria at microsatellite loci; however, litters sired by extra-colony males exhibited increased heterozygosity. While we do not have the data that refute a relationship between individual levels of inbreeding (Hs) and fitness, we propose that a combination of both male and female factors most likely explain the adaptive significance of extra-pair mating whereby common mole-rats maximize offspring fitness by detecting genetic compatibility with extra-pair mates at other key loci, but it is not known which sex controls these matings.     

Extra-pair paternity is not repeatable between years in Pied Flycatchers (Ficedula hypoleuca): a role for social context

Extra-pair paternity (EPP) is the consequence of the interactions between a social pair and extra-pair males during the female's fertile phase in a specific social context and ecological environment. Although EPP occurs in many avian species, there is a lack of understanding of how environmental factors may impact its frequency. Accordingly, the relative importance of individual characteristics on the one hand, and of their immediate social environment on the other, may affect EPP repeatability and thereby the capacity of this trait to respond to selection. If EPP is an individual genetically based trait that may respond to selection, we expect it to be repeatable across breeding seasons. To check this possibility, we analysed the within-individual repeatability in EPP of breeding males and females in two natural populations of Pied Flycatchers Ficedula hypoleuca in central Spain during three field seasons. We then studied the relationship between EPP and individual male and female traits (only some of which were themselves repeatable), as well as key context variables such as breeding synchrony and population density. Our results showed no repeatability for EPP in either sex. We found a positive association with laying date and stronger associations of EPP with male plumage and morphological traits than with female characteristics. We suggest that the variable social environment is an important modulator of EPP patterns, and that differences between field EPP studies in this respect may explain contradictory results in the same species, even in the same populations in different years.     

Sex-specific differential survival of extra-pair and within-pair offspring in song sparrows, Melospiza melodia

It is widely hypothesized that the evolution of female extra-pair reproduction in socially monogamous species reflects indirect genetic benefits to females. However, a critical prediction of this hypothesis, that extra-pair young (EPY) are fitter than within-pair young (WPY), has rarely been rigorously tested. We used 18 years of data from free-living song sparrows, Melospiza melodia, to test whether survival through major life-history stages differed between EPY and WPY maternal half-siblings. On average, survival of hatched chicks to independence from parental care and recruitment, and their total lifespan, did not differ significantly between EPY and WPY. However, EPY consistently tended to be less likely to survive, and recruited EPY survived for significantly fewer years than recruited WPY. Furthermore, the survival difference between EPY and WPY was sex-specific; female EPY were less likely to survive to independence and recruitment and lived fewer years than female WPY, whereas male EPY were similarly or slightly more likely to survive and to live more years than male WPY. These data indicate that extra-pair paternity may impose an indirect cost on females via their female offspring and that sex-specific genetic, environmental or maternal effects may shape extra-pair reproduction.     

Extra-pair paternity in the strongly monogamous Wandering Albatross Diomedea exulans has no apparent benefits for females

Although 92% of avian species are socially monogamous, extra-pair copulation (EPC), resulting in extra-pair paternity (EPP), is a common reproductive strategy in birds. Among seabirds, in which the rate of social monogamy reaches 100%, Procellariiformes (albatrosses and petrels) show low EPP rates, with the noticeable exception of the only albatross investigated in this regard, the Waved Albatross Phoebastria irrorata . This species, in which forced copulations are known to occur, showed a surprisingly high rate of EPP (25% of chicks). We investigate here EPP rates in another albatross species, the Wandering Albatross Diomedea exulans , subject to a demographic survey conducted for 38 years. We combined data on pair bonds with analysis of ten microsatellite loci and found that 10.7% of 75 chicks had an extra-pair sire. Although there was some evidence for inbreeding avoidance, within-pair and extra-pair chicks showed similar levels of heterozygosity, and the incidence of EPP was independent of age, experience or past reproductive success. Hence, we found no evidence that females benefit from EPCs. Owing to the male-biased sex ratio in adults, widowed and divorced males required more time to find a new mate (+28 and +72%, respectively) than did females. Combined with high sexual size dimorphism, this phenomenon might promote the forced copulations observed in this species. Our data therefore suggest that EPC is beneficial to unpaired males but occurs at random in females, consistent with the hypothesis that EPP results solely from forced EPCs. However, the importance of the latter for EPP and the part played by solitary males require further investigation.     

How female reed buntings benefit from extra-pair mating behaviour: testing hypotheses through patterns of paternity in sequential broods

Extra-pair paternity is an important aspect of reproductive strategies in many species of birds. Given that in most species females control whether fertilization occurs, they are expected to benefit in some way from the extra-pair matings. In this study we use patterns of extra-pair paternity (EPP) in broods of individual reed buntings (Emberiza schoeniclus), both within and between seasons, to test four hypothesized female benefits: (1) assessing potential future partners and seeking (2) genetic diversity (3) good genes, or (4) compatible genes. Reed buntings are socially monogamous, multibrooded passerines with extremely high levels of extra-pair paternity. We studied a population of reed buntings in the Netherlands in 2002 and 2003; 51% of offspring in 74% of nests were extra-pair. We showed that patterns of EPP did not support the first and second hypotheses, since females did not form a pair with previous extra-pair partners, EPP was not evenly distributed among broods and more broods than expected were sired by a single male. Furthermore, there was no relation between a male's within- and extra-pair fertilization success, no consistency in EPP between breeding attempts, no effect of parental relatedness on EPP and several cases of reciprocal paternity. These patterns do not support the good genes hypothesis and are most consistent with the genetic compatibility hypothesis. However, our previous finding that older males are more successful in gaining EPP, suggests some effect of good genes. These hypotheses need not be mutually exclusive, as females may select compatible males above a certain quality threshold (e.g. old males).     

Steller Sex: Infidelity and Sexual Selection in a Social Corvid (Cyanocitta stelleri)

Genetic analysis of avian mating systems has revealed that more than 70% of monogamous species show incidence of offspring parentage that does not match the social partner. Extra-pair parentage (EPP) has been linked to a variety of factors, including size and symmetry of ornamental traits, coloration, resource availability, and local conspecific density. We examined how ornamental plumage traits of individual Steller''s jays (Cyanocitta stelleri) and territory characteristics influence genetic fidelity of socially monogamous pairs. We used seven highly polymorphic microsatellite markers to assign paternity to 79 offspring, and identified 12 (15.2%) as extra-pair young (EPY). Steller''s jays with extra-pair young had significantly lower values of feather brightness and hue, indicating more ultraviolet-blue shifted coloration, and nested in closer proximity to the forest edge than Steller''s jays with no detected EPY. Body size, crest height, asymmetry of ornamental crest stripes, as well as vegetative composition of territories and their proximity to supplemental feeders appeared to have little relationship to EPP. These results indicate that extra-pair parentage plays a role in the evolution of secondary sexual characteristics in both sexes, and suggest local density and availability of resources may influence Steller''s jay mating dynamics.     

Extra-pair paternity in relation to regional and local climate in an Arctic-breeding passerine

Reproductive processes are affected by local and regional climate variation. Birds breeding in the Arctic may experience strong energetic constraints, which will affect their reproductive output. Recent research has emphasized the importance of extra-pair copulation as a means of improving reproductive output. In this paper, we explore ecological and climatic determinants that may explain variation in extra-pair paternity (EPP) in an arctic-breeding passerine, the snow bunting Plectrophenax nivalis. EPP occurred in 10.8 % of the young and 20.9 % of the broods sampled from 1999 to 2003. We found that the proportion of extra-pair young in a nest was positively related to the body size and age of the social male and weakly negatively related to the local average minimum temperature prior to the onset of egg laying. These results suggest that older and larger males lost a larger share of paternity than smaller and younger males, and that the relative loss of paternity decreased with cold weather during the female’s fertile period. Large and old males spend less time mate guarding compared to small and young males and may allocate more time towards extra-pair forays, and thus lose more paternity in their own nest. Climatic conditions most likely constrain the total energy budget with less energy available for extra-pair activity in cold weather.     

Genotype and extra-pair paternity in the house wren: a rare-male effect?

Females in socially monogamous species may select extra-pair (EP) mates to increase the heterozygosity, and hence fitness, of their offspring. We tested this hypothesis in the house wren (Troglodytes aedon), a largely monogamous songbird in which EP young are common. We typed paired males and females, nestlings, and males on neighbouring territories, at five to seven microsatellite loci over 2 years in a Wyoming, USA, population. We identified EP sires at 20 nests with EP young. In pairwise comparisons, we found no significant differences between cuckolded within-pair (WP) males and EP sires in three measures of heterozygosity (mean d2, standardized heterozygosity and internal relatedness). However, EP sires had fewer alleles that were common within the population than did the WP males they cuckolded. Nearby males who were EP sires also had fewer common alleles than did nearby males who did not sire EP young. Females in our population may be more prone to accept copulations from males with rare genotypes than from males with common genotypes. Alternatively, selection of rare-male sperm may occur within the female reproductive tract. Because mating with rare males is likely to increase offspring heterozygosity, our data suggest that EP mating may provide genetic benefits to females.     

Female house wrens (Troglodytes aedon) increase the size, but not immunocompetence, of their offspring through extra-pair mating

House wrens are typically socially monogamous, but frequently engage in extra-pair matings leading to multisired broods. Because females do not appear to acquire direct material benefits from their extra-pair mates, we tested the hypothesis that female house wrens derive indirect genetic benefits, such as enhanced immunocompetence (cutaneous immune activity, humoral immunity, and plasma bactericidal activity) and condition (size and haematoserological traits) for their offspring, by mating polyandrously. We predicted that extra-pair young (EPY) should show greater immune responsiveness and better body condition than their within-pair maternal half-siblings (WPY). Contrary to our prediction, WPY had higher cutaneous immune activity than their EPY brood-mates in two of three years, and EPY and WPY did not differ in measures of innate and humoral immunity. WPY also had higher albumin to γ-globulin ratios than EPY; however, they were not in better condition based on other measures. EPY had consistently longer tarsi (a measure of long-bone size) than their WPY half-siblings, suggesting that females engage in extra-pair copulations with larger males. The benefits of large structural size in the study population is unknown, but based on evidence from other passerines, we suggest that structural size may be an important fitness-related trait in house wrens. We conclude that our results are not consistent with the hypothesis that females gain immune-related benefits for their offspring by engaging in extra-pair matings. Further study of the fitness consequences of differences in tarsus length is needed to determine whether females acquire size-related benefits for their offspring from extra-pair mates.     

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.