Rates Of Extra-group Paternity Research Articles

Male condition and group heterogeneity predict extra-group paternity in a Neotropical bat

Extra-group paternity, in which offspring are sired by a male outside the breeding group, may alter the distribution of reproductive success in a population, thus affecting the opportunity for sexual selection. Both inter- and intraspecific studies have focused largely on mating systems in which females choose their social mates, and less is known about extra-group paternity in polygynous systems in which social mates are largely dictated by male-male competition. In this study, we examine the frequency and distribution of extra-group paternity in a harem-forming bat, Phyllostomus hastatus. We find that despite aggressive harem defense, males are unable to fully monopolize reproduction within their harem and over 70% of harems contain extra-group offspring. Harem males in better body condition suffered less paternity loss, but we found no effect of male age or body size. Even though the age and size of individual females did not predict offspring paternity, we found a significant effect of age heterogeneity within the group. Harems composed of differently aged females were more likely to contain extra-group offspring. Our results not only provide evidence for the role of male defense in preventing extra-group paternity but also suggest that social group composition has consequences for male reproductive success. In polygynous societies, the ability to monopolize mating is critical to reproductive success. As the group size increases, defense often becomes more difficult, resulting in increased rates of extra-group paternity. We find that among greater spear-nosed bats, extra-group offspring occur in most harems, but the overall rate of extra-group paternity is relatively low despite their large harems (15–30 females). Variation in the rate of extra-group paternity between harems is explained by male body condition (i.e., relative mass) but not harem size. Additionally, the rate of extra-group paternity is not explained entirely by male attributes, as we find that age heterogeneity within the female group is a significant predictor of the extra-group paternity rate. Our results support the hypothesis that not only the physical condition of a male influences his ability to monopolize reproduction but also the group composition influences the female mating behavior.

Long-term analysis on the variance of extra-group paternities in rhesus macaques

Extra-group paternity (EGP) has been described in various mammalian species; however, little is known about which factors contribute to the variation in EGP, as the majority of studies were restricted in time and the number of groups considered. Using longitudinal demographic and genetic data, we aim to investigate which factors predict rates of EGP in the free-ranging rhesus macaque population of Cayo Santiago, Puerto Rico (USA). Of the 1649 infants considered which were born into six social groups over 9 years, we identified an average of 16% of infants resulting from EGPs. We tested the influence of group size, breeding group sex ratio, female reproductive synchrony, and group instability on the occurrence of EGPs. Our results suggest a tendency for EGPs to increase as the proportion of females increased in larger groups, but no such effect in smaller groups. Furthermore, as group instability and female reproductive synchrony decreased, the number of EGPs tended to increase. Our results support the hypothesis that group structure affects the occurrence of EGPs, which might be mediated by male mating opportunities, male monopolization potential, and/or female choice.Significance statementIn several species, both sexes seek alternative reproductive strategies to enhance their reproductive success. For instance, females may pursue EGPs to potentially increase genetic compatibility with males, or males may seek EGPs to improve their mating opportunities. Our longitudinal analysis, including demographic and genetic data over 9 years of six social groups of rhesus macaques, revealed high variation in the occurrence of EGPs across groups and years, and this variation tended to depend on group characteristics such as breeding group size, sex ratio, female synchrony, and group instability. The data suggest that group structure affects the number of EGPs in this group-living primate. Our results show that EGPs can affect the distribution of paternity within social groups and should be taken into account when assessing reproductive success.

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.

Neighbouring-group composition and within-group relatedness drive extra-group paternity rate in the European badger (Meles meles).

Extra-group paternity (EGP) occurs commonly among group-living mammals and plays an important role in mating systems and the dynamics of sexual selection; however, socio-ecological and genetic correlates of EGP have been underexplored. We use 23 years of demographic and genetic data from a high-density European badger (Meles meles) population, to investigate the relationship between the rate of EGP in litters and mate availability, mate incompatibility and mate quality (heterozygosity). Relatedness between within-group assigned mothers and candidate fathers had a negative quadratic effect on EGP, whereas the number of neighbouring-group candidate fathers had a linear positive effect. We detected no effect of mean or maximum heterozygosity of within-group candidate fathers on EGP. Consequently, EGP was associated primarily with mate availability, subject to within-group genetic effects, potentially to mitigate mate incompatibility and inbreeding. In badgers, cryptic female choice, facilitated by superfecundation, superfoetation and delayed implantation, prevents males from monopolizing within-group females. This resonates with a meta-analysis in group-living mammals, which proposed that higher rates of EGP occur when within-group males cannot monopolize within-group females. In contrast to the positive meta-analytic association, however, we found that EGP associated negatively with the number of within-group assigned mothers and the number of within-group candidate fathers; potentially a strategy to counter within-group males committing infanticide. The relationship between the rate of EGP and socio-ecological or genetic factors can therefore be intricate, and the potential for cryptic female choice must be accounted for in comparative studies.

A molecular analysis of African lion (Panthera leo) mating structure and extra‐group paternity in Etosha National Park

The recent incorporation of molecular methods into analyses of social and mating systems has provided evidence that mating patterns often differ from those predicted by group social organization. Based on field studies and paternity analyses at a limited number of sites, African lions are predicted to exhibit a strict within-pride mating system. Extra-group paternity has not been previously reported in African lions; however, observations of extra-group associations among lions inhabiting Etosha National Park in Namibia suggest deviation from the predicted within-pride mating pattern. We analysed variation in 14 microsatellite loci in a population of 164 African lions in Etosha National Park. Genetic analysis was coupled with demographic and observational data to examine pride structure, relatedness and extra-group paternity (EGP). EGP was found to occur in 57% of prides where paternity was analysed (n = 7), and the overall rate of EGP in this population was 41% (n = 34). Group sex ratio had a significant effect on the occurrence of EGP (P < 0.05), indicating that variation in pride-level social structure may explain intergroup variation in EGP. Prides with a lower male-to-female ratio were significantly more likely to experience EGP in this population. The results of this study challenge the current models of African lion mating systems and provide evidence that social structure may not reflect breeding structure in some social mammals.

Male-Mediated Gene Flow in Patrilocal Primates

BackgroundMany group–living species display strong sex biases in dispersal tendencies. However, gene flow mediated by apparently philopatric sex may still occur and potentially alters population structure. In our closest living evolutionary relatives, dispersal of adult males seems to be precluded by high levels of territoriality between males of different groups in chimpanzees, and has only been observed once in bonobos. Still, male–mediated gene flow might occur through rare events such as extra–group matings leading to extra–group paternity (EGP) and female secondary dispersal with offspring, but the extent of this gene flow has not yet been assessed.Methodology/Principal FindingsUsing autosomal microsatellite genotyping of samples from multiple groups of wild western chimpanzees (Pan troglodytes verus) and bonobos (Pan paniscus), we found low genetic differentiation among groups for both males and females. Characterization of Y–chromosome microsatellites revealed levels of genetic differentiation between groups in bonobos almost as high as those reported previously in eastern chimpanzees, but lower levels of differentiation in western chimpanzees. By using simulations to evaluate the patterns of Y–chromosomal variation expected under realistic assumptions of group size, mutation rate and reproductive skew, we demonstrate that the observed presence of multiple and highly divergent Y–haplotypes within western chimpanzee and bonobo groups is best explained by successful male–mediated gene flow.Conclusions/SignificanceThe similarity of inferred rates of male–mediated gene flow and published rates of EGP in western chimpanzees suggests this is the most likely mechanism of male–mediated gene flow in this subspecies. In bonobos more data are needed to refine the estimated rate of gene flow. Our findings suggest that dispersal patterns in these closely related species, and particularly for the chimpanzee subspecies, are more variable than previously appreciated. This is consistent with growing recognition of extensive behavioral variation in chimpanzees and bonobos.

Low genetic variability, female‐biased dispersal and high movement rates in an urban population of Eurasian badgers Meles meles

1. Urban and rural populations of animals can differ in their behaviour, both in order to meet their ecological requirements and due to the constraints imposed by different environments. The study of urban populations can therefore offer useful insights into the behavioural flexibility of a species as a whole, as well as indicating how the species in question adapts to a specifically urban environment. 2. The genetic structure of a population can provide information about social structure and movement patterns that is difficult to obtain by other means. Using non-invasively collected hair samples, we estimated the population size of Eurasian badgers Meles meles in the city of Brighton, England, and calculated population-specific parameters of genetic variability and sex-specific rates of outbreeding and dispersal. 3. Population density was high in the context of badger densities reported throughout their range. This was due to a high density of social groups rather than large numbers of individuals per group. 4. The allelic richness of the population was low compared with other British populations. However, the rate of extra-group paternity and the relatively frequent (mainly temporary) intergroup movements suggest that, on a local scale, the population was outbred. Although members of both sexes visited other groups, there was a trend for more females to make intergroup movements. 5. The results reveal that urban badgers can achieve high densities and suggest that while some population parameters are similar between urban and rural populations, the frequency of intergroup movements is higher among urban badgers. In a wider context, these results demonstrate the ability of non-invasive genetic sampling to provide information about the population density, social structure and behaviour of urban wildlife.

Female reproductive synchrony predicts skewed paternity across primates.

Recent studies have uncovered remarkable variation in paternity within primate groups. To date, however, we lack a general understanding of the factors that drive variation in paternity skew among primate groups and across species. Our study focused on hypotheses from reproductive skew theory involving limited control and the use of paternity “concessions” by investigating how paternity covaries with the number of males, female estrous synchrony, and rates of extragroup paternity. In multivariate and phylogenetically controlled analyses of data from 27 studies on 19 species, we found strong support for a limited control skew model, with reproductive skew within groups declining as female reproductive synchrony and the number of males per group increase. Of these 2 variables, female reproductive synchrony explained more of the variation in paternity distributions. To test whether dominant males provide incentives to subordinates to resist matings by extragroup males, that is, whether dominants make concessions of paternity, we derived a novel prediction that skew is lower within groups when threat from outside the group exists. This prediction was not supported as a primary factor underlying patterns of reproductive skew among primate species. However, our approach revealed that if concessions occur in primates, they are most likely when female synchrony is low, as these conditions provide alpha male control of paternity that is assumed by concessions models. Collectively, our analyses demonstrate that aspects of male reproductive competition are the primary drivers of reproductive skew in primates.

Differing rates of extra-group paternity between two populations of the Australian magpie (Gymnorhina tibicen)

Extra-pair paternity (EPP) is a common feature of the mating systems of many birds. The rate of EPP may vary between species, races and populations. A comparison of extra-group paternity (EGP) rates was made between two races of a group-living passerine, the Australian magpie (Gymnorhina tibicen), to determine if similar mating systems were being employed. The two populations had similar social structure, but differed in group size and dispersal. It was predicted that dispersal differences would have a profound effect on the rate of EGP between the populations, as the population with the lower rate of dispersal and higher chance of breeding with a close relative would engage in EGPs more frequently. Eight microsatellite loci were used to determine parentage in the white-backed Australian magpie (G. t. tyrannica). The rate of EGP was found to be 44%. Dispersal rates were estimated from observational data. Over half of the juvenile magpie cohort from the previous breeding season left the territorial group. These results contrast sharply with the results found by other researchers in a population of western Australian magpies (G. t. dorsalis). In this population, 82% EGP is recorded and dispersal of juveniles is close to nil. The results indicate that dispersal rate is a potentially important predictor of rates of extra-group fertilisations between populations of this species, and suggest that females maximise their reproductive output by avoiding breeding with close kin.

Paternity and relatedness in wild chimpanzee communities.

The genetic structure of three contiguous wild chimpanzee communities in West Africa was examined to determine the extent to which the community, the mixed-sex social unit of chimpanzees, represents a closed reproductive unit. An analysis of paternity for 41 offspring resulted in 34 cases of paternity assignment to an adult male belonging to the same community. Among the 14 offspring for which all potential within-community fathers have been tested, one likely case of extra-group paternity (EGP) has been identified, suggesting an incidence of EGP of 7%. This more extensive analysis contradicts a previous genetic study of the Tai chimpanzees that inferred 50% extra-group fathers. We suggest, based on direct comparison of results for 33 individuals at 1 microsatellite locus and direct comparison of paternity assignments for 11 offspring, that the error rate in the previous study was too high to produce accurate genotypes and assignments of paternity and hence caused the false inference of a high rate of EGP. Thus, the community is the primary but not exclusive unit for reproduction in wild chimpanzees, and females do not typically reproduce with outside males. Despite the inferred low level of gene flow from extra-community males, relatedness levels among the community males are not significantly higher than among community females, and the distribution of genetic relationships within the group suggests that, rather than a primarily male-bonded social structure, the group is bonded through relationships between males and females. Kinship may explain cooperative behaviors directed against other communities, but is unlikely to explain the high levels of affiliation and cooperation seen for male within-community interactions.