Patterns Of Extra-pair Paternity Research Articles

Extra‐pair paternity enhances the reproductive fitness of urban Chinese blackbird

Urbanization is a human‐induced process of rapid habitat change that can affect the reproductive success of animals. The occurrence of extra‐pair paternity (EPP) may be sensitive to changes in urban ecological conditions. In this study, the Chinese blackbird Turdus mandarinus, a common breeding bird in southern Chinese cities, was selected as the focus species to explore the EPP patterns of monogamous birds in developing cities and the relationship between pairs. Over four breeding seasons, 316 Chinese blackbird nestlings and 20 adults in both urban and rural areas were monitored and genotyped for 11 microsatellite loci to determine progeny affinity. We confirmed that both the brood size and hatching rate of EPP nests were significantly larger than those of within‐pair paternity (WPP) nests. The body mass, beak length, head length, and body length of 12‐day age extra‐pair offspring (EPO) were significantly greater than those of within‐pair offspring (WPO), suggesting important benefits of EPP. However, in accordance with the analyses of nest ecological variables, we concluded that EPP occurs most often in areas with low urbanization levels, indicating some constraints for this reproductive strategy in cities. Our findings provide new insights about how this growing human‐induced landscape change affects mating behaviour in birds, an important aspect in avian ecology and evolution.

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.

Extra-pair paternity in a species with frequent extra-pair courtship feedings, few extra-pair copulations, and male-biased parental care

Patterns of extra pair paternity (EPP) and intraspecific brood parasitism (IBP) were studied in a Whiskered Tern Chlidonias hybrida population characterized by female brood desertion, a high level of extra pair courtship feedings (10%) and a low level of extra pair copulation (EPC; 0.6%). In this study, we used a set of microsatellite loci to analyse parentage in 56 Whiskered Tern families from southern Poland. Depending on the method, we detected that 1.4%–3.6% of chicks were sired by an extra-pair male, and extra-pair chicks were present in 3.6%–8.9% of broods. IBP was observed in 8.9%–14.3% of broods, corresponding to 3.6%–6.4% of the chicks. The low rate of EPP is in agreement with the hypothesis that in species with high male parental investment, females should avoid EPC. The low level of IBP indicates that intraspecific egg dumping is not a common female strategy in Whiskered Tern, similar to many other colonial waterbird species.

Extra‐pair paternity in Blue Tits (Cyanistes caeruleus) depends on the combination of social partners' age

There is growing evidence that engaging in extra‐pair copulations may be a strategy by which females can modify their initial mate choice if they are constrained by primary choice of the social mate. Several factors such as genetic similarity and adult phenotypic traits can affect extra‐pair paternity (EPP) patterns, but the relative importance of these factors may vary among species. Moreover, interactive effects of male and female characteristics have rarely been considered. Here, we aimed to study how multiple parameters characterizing a breeding pair (i.e. genetic similarity between mates, partners’ age and laying date) predict the occurrence of EPP at the brood level. The study uses 4 years of data from a wild population of Blue Tits Cyanistes caeruleus. Contrary to predictions of the inbreeding avoidance hypothesis, we did not find a positive relationship between the occurrence of EPP and the relatedness of social mates. We also found that the probability of EPP was unrelated to laying date. However, EPP was predicted by an interaction of social partners' ages. Specifically, EPP was less likely when old females were paired with old males in comparison to old females paired to young males. Our study suggests that the occurrence of EPP may be the result of behavioural interactions in which both male and female age are important for determining the outcome. Our results confirm the importance of considering the interactions of male and female characteristics in studies investigating EPP patterns.

Winter associations predict social and extra-pair mating patterns in a wild songbird.

Despite decades of research, our understanding of the underlying causes of within-population variation in patterns of extra-pair paternity (EPP) remains limited. Previous studies have shown that extra-pair mating decisions are linked to both individual traits and ecological factors. Here, we examine whether social associations among individuals prior to breeding also shape mating patterns, specifically the occurrence of EPP, in a small songbird, the blue tit. We test whether associations during the non-breeding period predict (1) future social pairs, (2) breeding proximity (i.e. the distance between breeding individuals) and (3) the likelihood that individuals have extra-pair young together. Individuals that were more strongly associated (those that foraged more often together) during winter tended to nest closer together. This, by itself, predicts EPP patterns, because most extra-pair sires are close neighbours. However, even after controlling for spatial effects, female–male dyads with stronger social associations prior to breeding were more likely to have extra-pair young. Our findings reveal a carry-over from social associations into future mating decisions. Quantifying the long-term social environment of individuals and studying its dynamics is a promising approach to enhance our understanding of the process of (extra-)pair formation.

Extra-pair paternity patterns in European barn swallows Hirundo rustica are best explained by male and female age rather than male ornamentation

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

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.

Extra-pair paternity in a long-distance migratory songbird beyond neighbors’ borders and across male age classes

Roughly 90% of socially monogamous bird species exhibit some degree of extra-pair paternity (EPP), although the extent and the underlying mechanisms vary among species. We analyzed spatial and demographic patterns of EPP over a 6 year period (2005–2010) as part of a long-term population study of Canada Warblers (Cardellina canadensis (L., 1766)). We identified 12 microsatellite loci used to assess paternity for 185 nestlings from 61 nests. Extra-pair young (EPY) accounted for 41.6% of all nestlings and 57.4% of nests contained at least one EPY. Fewer than half of EPY were sired by males who shared territorial boundaries, and some males sired young in nests 1 km from their territory. The age of social males did not differ from males who cuckolded them. The majority (83%) of EPY were sired by males in older age classes (2+ years old), while <17% were sired by 1 year olds. Of the young sired by older males, 58.5% were sired by males 3–7 years old. Males that sired more EPY sired fewer within-pair young (WPY); those without EPY sired more WPY suggesting a possible fitness trade-off between these two strategies. Our findings suggest multiple age-based strategies within a single breeding population, as well as potential strategy shifts to maximize lifetime fitness as they age.

The colour of paternity: extra-pair paternity in the wild Gouldian finch does not appear to be driven by genetic incompatibility between morphs.

In socially monogamous species, individuals can use extra-pair paternity and offspring sex allocation as adaptive strategies to ameliorate costs of genetic incompatibility with their partner. Previous studies on domesticated Gouldian finches (Erythrura gouldiae) demonstrated a genetic incompatibility between head colour morphs, the effects of which are more severe in female offspring. Domesticated females use differential sex allocation, and extra-pair paternity with males of compatible head colour, to reduce fitness costs associated with incompatibility in mixed-morph pairings. However, laboratory studies are an oversimplification of the complex ecological factors experienced in the wild and may only reflect the biology of a domesticated species. This study aimed to examine the patterns of parentage and sex ratio bias with respect to colour pairing combinations in a wild population of the Gouldian finch. We utilized a novel PCR assay that allowed us to genotype the morph of offspring before the morph phenotype develops and to explore bias in morph paternity and selection at the nest. Contrary to previous findings in the laboratory, we found no effect of pairing combinations on patterns of extra-pair paternity, offspring sex ratio or selection on morphs in nestlings. In the wild, the effect of morph incompatibility is likely much smaller, or absent, than was observed in the domesticated birds. Furthermore, the previously studied domesticated population is genetically differentiated from the wild population, consistent with the effects of domestication. It is possible that the domestication process fostered the emergence (or enhancement) of incompatibility between colour morphs previously demonstrated in the laboratory.

Does nest predation risk affect the frequency of extra‐pair paternity in a socially monogamous passerine?

While considerable variations in both the frequency of extra‐pair paternity (EPP) and the behavioral events that produce it are recognized among species, populations, individuals, and breeding attempts, the determinants of these variations are surprisingly difficult to establish. Nest predation may be one such determinant, since it is the most important source of reproductive failure, and past studies have suggested a variety of reproductive flexibilities under nest predation risk. However, despite its potentially significant effect on mating behaviors, nest predation risk has rarely been discussed in association with variations in intraspecific EPP patterns. Here, we examined the effect of naturally occurring nest predation, which varied between sites, years, and breeding attempts, on patterns of EPP in 92 broods (132 adults and 710 nestlings) of the Japanese great tit Parus major minor. We found that the frequency of extra‐pair offspring was positively correlated with the nest predation rate, along with a correlation to breeding attempts in a season, but not with other factors such as individual quality or breeding density. Under high nest‐predation risk, it may be adaptive for males to search for additional extra‐pair copulation to spread the risk of losing all offspring and to invest less in mate‐guarding, which also enables females to seek additional extra‐mating. The results of this study suggest that nest predation risk, among other factors, may significantly influence paternity allocation in birds.

Effects of heterozygosity and MHC diversity on patterns of extra-pair paternity in the socially monogamous scarlet rosefinch

Extra-pair copulation without apparent direct benefits is an evolutionary puzzle that requires indirect fitness benefits to females to explain its ubiquity in socially monogamous mating systems. Using wild scarlet rosefinches (Carpodacus erythrinus), we tested if genetic benefits in the form of global (microsatellite) heterozygote advantage, adaptive genes (major histocompatibility complex), or complementary genes (using both markers) were responsible for female extra-pair mate choice, while considering that the benefits of mate choice may be conditional on female genotype. We found no evidence for assortative or relatedness-based mating (complementary genes), but higher MHC diversity, microsatellite heterozygosity, and condition were significantly related to male extra-pair paternity (EPP) success. In contrast, female probability of having extra-pair offspring decreased with increasing heterozygosity. Interestingly, extra-pair and within-pair males had higher heterozygosity than their female mates and extra-pair males had higher MHC supertype diversity. The only genetic difference between extra-pair and within-pair offspring was lower variance in MHC allelic diversity within extra-pair offspring, providing limited support for indirect genetic fitness benefits for the markers tested. Offspring had both higher neutral heterozygosity and number of MHC supertypes than adults, as well as significant identity disequilibrium, potentially suggesting that mates are chosen to increase offspring diversity in the period of the present study. Overall, our results point to an EPP heterozygote advantage for males, especially when involving less heterozygous females, and suggest that heterozygosity effects on reproduction may differ between the sexes.

Spatial patterns of extra-pair paternity: beyond paternity gains and losses.

Most studies on extra-pair paternity (EPP) focus either on a specific male's extra-pair gains or his extra-pair losses. For an individual bird however, mate choice or mate availability may underlie strong spatial restrictions. Disregarding this spatial aspect may underestimate or mask effects of parameters influencing observed EPP patterns. Here, we propose a spatially explicit model for investigating the probability of having extra-pair offspring (EPO) within local networks of breeding pairs. The data set includes all realized and unrealized potential extra-pair matings. This method is biologically meaningful because it allows (a) considering both members of an extra-pair mating and their social mates, and (b) direct modelling of the spatial context in which extra-pair behaviour occurs. The method has the advantage that it can provide inference about the relative contribution of spatial and non-spatial parameters, and about the relative importance of male and female neighbourhoods. We apply this method to parentage data from 1025 broods collected over 12 breeding seasons in two independent study populations of blue tits (Cyanistes caeruleus). We investigate a set of predictions based on the EPP literature, namely that EPP depends on male age and body size, breeding density and breeding synchrony. In all analyses, we control for breeding distance, a parameter that is expected to influence EPP even under random mating. The results show that older and larger males were more likely to sire EPO, but both effects decreased with increasing breeding distance. Local breeding density but not synchrony predicted whether a particular male-female combination had EPO, at least in one of the study areas. Apart from breeding distance, male age had the strongest effect on EPP, followed by a measure of breeding density. The method thus allows a comprehensive assessment of the relative importance of different types of spatial and non-spatial parameters to explain variation in the occurrence of EPP, while controlling for the fact that individuals that breed further apart are less likely to have EPO. The proposed approach is not limited to investigate EPP, but can be applied to other behavioural interactions between two individuals, such as dominance, competition and (social) mating.

Multiple sexual pigments, assortative social pairing, and genetic paternity in the yellow warbler (Setophaga petechia)

In socially monogamous species, extra-pair paternity may increase the reproductive success of highly ornamented males, mediating the evolution of sexual ornaments. However, ornaments may also attract social mates, and a tradeoff between extra-pair paternity (EPP) and within-pair paternity (WPP) may complicate mating strategies. Further, in many socially monogamous species, females are also ornamented, and the relationship between female ornamentation and patterns of EPP has been neglected. We investigated the patterns of genetic paternity with respect to carotenoid- and melanin-based pigmentation in yellow warblers (Setophaga petechia) of both sexes. We asked whether males face tradeoffs between EPP and WPP, how paternity patterns relate to carotenoid- versus melanin-based pigmentation, and whether less EPP occurs in broods when males and females are assortatively paired. Males faced a tradeoff between EPP and WPP. Moreover, non-additive relationships existed between paternity patterns and the two pigment types in both sexes. Males with high melanin coverage but dull carotenoid pigmentation achieved EPP but lost WPP, whereas males with high levels of both pigment types had high WPP but gained little EPP. A parallel pattern occurred in females. Warblers paired assortatively by pigmentation and EPP was less common in broods when the sexes were assortatively paired by carotenoid pigmentation. Results suggest that the most colorful birds obtain high quality social mates and advance reproductive success through WPP, show that correlations can arise between female ornamentation and patterns of EPP, and also uniquely suggest that social pairing patterns may influence extra-pair mating strategies.

Extra-pair paternity in two sympatric Aegithalos tits: patterns and implications

The explanation for extra-pair paternity (EPP) variation continues to attract research interest in the area of avian breeding systems. Comparisons among closely related species are recommended to explore factors that affect EPP rate variations. We utilised microsatellite markers to investigate extra-pair paternity in two sympatric populations of congeneric Black-throated Tits, Aegithalos concinnus, and Silver-throated Tits, A. glaucogularis. The two species share a similar breeding period at our study site and have helpers during breeding at some nests. The results suggest that the two species had low levels of extra-pair paternity: 5.7 % of the offspring in the Black-throated Tits and 6.8 % of the offspring in the Silver-throated Tits. The proportion of broods with extra-pair paternity in the Silver-throated Tits (33.3 %) was higher overall than the Black-throated Tits (17.2 %). This difference is consistent with the prediction by their different male attendance of incubation, but failed to be explained by major ecological factors. On the one hand, we conducted the study at the same site during the same time, which therefore limited the potential effect of different environmental conditions and habitat on their EPP incidence. On the other hand, other factors such as the inter-nest distances failed to explain the observed pattern. Current results also could not rule out an effect of evolutionary history on the EPP patterns of these two related species. Our research on their cooperative breeding system found a low proportion of cooperative breeding nests with offspring sired by helpers (Black-throated Tit, 8.3 % and Silver-throated Tit, 25.0 %), indicating that a direct reproductive benefit is not a likely major reason for the existence of the helpers in these two species.

Male decisions or female accessibility? Spatiotemporal patterns of extra pair paternity in a songbird

Extra pair paternity is widespread in birds, but its high variability across years, populations, and species is to a great extent unresolved. Here we explored, during 2 breeding seasons, population and individual accessibility to fertile females at different spatiotemporal scales in a population of pied flycatchers (Ficedula hypoleuca) to understand whether individual patterns of extra pair paternity were due to adaptive individual behavior or ecological constraints. Our aim was to comprehend variation in extra pair paternity population patterns through the understanding of individual behavior. At the population level, extra pair paternity probability decayed with distance between nests. At the individual level, however, males engaged in extra pair paternity with distant (up to 390 m) females despite the fact that there were often fertile females in closer territories. Extra pair paternity cases occurred mostly during egg laying and the incubation of the extra pair male’s social female despite that other neighboring females were fertile before and after these periods. Results suggest a male strategy to maximize reproductive output by guarding their social females during their peak of fertility, seeking extra pair paternity afterwards and investing in parental duties once their social nestlings hatch. This may explain why extra pair paternity rate was higher in the year with lower breeding synchrony, because this allowed early-breeding males to have more extra pair paternity opportunities after their social mate laying onset. This study highlights the necessity of considering the social contexts of individuals at the spatiotemporal scales at which extra pair paternity takes place to understand variation in extra pair paternity patterns at the individual and population levels.

Natural extrapair paternity matches receptivity patterns in unguarded females: evidence for importance of female choice

While observational and experimental field studies have demonstrated that extrapair paternity is associated with a variety of male traits, there are still few published studies associating measures of paternity with behavioural preferences of females for extrapair males. In this sense, the majority of studies of extrapair paternity have failed to separate male competition from female choice. In this study we compared patterns of extrapair paternity in western bluebirds, Sialia mexicana, to previously published data on extrapair mating preferences from the same population. Results from previous experiments, where females’ mates were prevented from guarding or otherwise interfering with extrapair mating, accurately predicted patterns of paternity at 256 unmanipulated nests examined over a 6-year period. Specifically, as predicted based on which males were accepted as extrapair copulation partners, genetic extrapair sires were older but not larger than a female’s social mate. At the same time, relatively older extrapair males were not proportionally more successful, in terms of proportion of offspring sired, than younger males. Together these findings indicate that female choice for older males is expressed, but male competition, sperm competition and intersexual conflict also influence the magnitude of paternity. We suggest that experimental approaches, combined with measures of paternity under unmanipulated conditions, provide important opportunities to test the potential role of male versus female behaviours as selective factors in extrapair fertilizations.

Who initiates extrapair mating in song sparrows?

Extrapair paternity (EPP) is a common feature of many mating systems. Although molecular methods have made it possible to document the rate of EPP across numerous taxa, we still lack an understanding of how and why EPP happens. Behavioral data on mating interactions are needed to answer this question. We employed radiotelemetry to follow the movement patterns of tagged song sparrows (Melospiza melodia) during their nesting cycle. We found that females and males commonly forayed onto neighboring territories in the prefertile period, frequently together. In the fertile period, however, the foray rate dropped significantly, and females largely stayed on their own territories. Concurrently in the fertile period, both the time mates spent in proximity and intrusion rates on their territories increased compared with the prefertile period. After the female started laying eggs, proximity of the mates to one another declined again, and some males started to foray onto neighboring territories, in most cases into territories where there was a fertile female. Thus, females do not seem to seek out particular males for extrapair copulations (EPCs) in their fertile period, but rather it is the males who actively seek extrapair mating. Males therefore face a trade-off between ensuring paternity at home and pursuing copulations elsewhere. Agonistic interactions between extrapair males and females were almost entirely absent, suggesting that males do not force females into copulations. Therefore, in song sparrows, males have to initiate EPCs by seeking out fertile females, suggesting that males probably drive the pattern of EPP in our

Comprehensive paternity assignment: genotype, spatial location and social status in song sparrows, Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra-pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6-day-old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra-pair sires primarily occupied territories neighbouring their extra-pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra-pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.

Extrapair paternity in a flock‐living passerine, the vinous‐throated parrotbill Paradoxornis webbianus

Understanding the factors that affect the occurrence of extrapair paternity (EPP) is one of the central issues in sexual selection. We investigated genetic parentage and the ecological factors affecting patterns of EPP in the vinous‐throated parrotbill, Paradoxornis webbianus, a flock‐living species with double broods. Using microsatellite DNA fingerprinting, we determined parentage of 246 offspring in 50 broods over two years (2005 and 2006). Nineteen offspring (8%) from 13 broods (26%) were sired by extrapair males and one offspring (0.4%) was probably the result of intraspecific brood parasitism. The prevalence of EPP varied significantly through the breeding season: 95% of broods with EPP (12/13) occurred in the first of two laying peaks. Parentage assignment revealed that half of extrapair males (6/12) were adjacent neighbours. The distribution of EPP was not significantly related to the ecological factors including breeding density and breeding synchrony. Instead, we suggest that social characteristics such as flocking and weak territoriality may determine the observed pattern of EPP in this study.

The genetic similarity between pair members influences the frequency of extrapair paternity in alpine marmots

Extrapair paternity is widespread in birds and mammals. In particular, the alpine marmot, Marmota marmota, has a high frequency of extrapair paternity that seems to be explained by the genetic compatibility hypothesis. We investigated whether the number and proportion of extrapair young depend on the heterozygosity (individual genetic diversity) of the social male, or on the genetic similarity between the social male and his mate (relatedness). Both the number and the proportion of extrapair young increased with both high similarity and dissimilarity between the social pair. In combination with previous results, our study suggests that patterns of extrapair paternity in alpine marmots can best be explained by the genetic compatibility hypothesis, and more precisely its optimal outbreeding variant. Our results indeed suggest that extrapair paternity is a mechanism to avoid both in- and outbreeding depression. We discuss which proximal mechanisms may be involved in extrapair paternity in this species.