Genetic population structure and relatedness in the narrow-striped mongoose (Mungotictis decemlineata), a social Malagasy carnivore with sexual segregation.
ABSTRACT: Information on the genetic structure of animal populations can allow inferences about mechanisms shaping their social organization, dispersal, and mating system. The mongooses (Herpestidae) include some of the best-studied mammalian systems in this respect, but much less is known about their closest relatives, the Malagasy carnivores (Eupleridae), even though some of them exhibit unusual association patterns. We investigated the genetic structure of the Malagasy narrow-striped mongoose (Mungotictis decemlineata), a small forest-dwelling gregarious carnivore exhibiting sexual segregation. Based on mtDNA and microsatellite analyses, we determined population-wide haplotype structure and sex-specific and within-group relatedness. Furthermore, we analyzed parentage and sibship relationships and the level of reproductive skew. We found a matrilinear population structure, with several neighboring female units sharing identical haplotypes. Within-group female relatedness was significantly higher than expected by chance in the majority of units. Haplotype diversity of males was significantly higher than in females, indicating male-biased dispersal. Relatedness within the majority of male associations did not differ from random, not proving any kin-directed benefits of male sociality in this case. We found indications for a mildly promiscuous mating system without monopolization of females by males, and low levels of reproductive skew in both sexes based on parentages of emergent young. Low relatedness within breeding pairs confirmed immigration by males and suggested similarities with patterns in social mongooses, providing a starting point for further investigations of mate choice and female control of reproduction and the connected behavioral mechanisms. Our study contributes to the understanding of the determinants of male sociality in carnivores as well as the mechanisms of female competition in species with small social units.
Project description:In group living animals, especially among primates, there is consistent evidence that high-ranking males gain a higher reproductive output than low-ranking males. Primate studies have shown that male coalitions and sociality can impact male fitness; however, it remains unclear whether males could potentially increase their fitness by preferentially supporting and socializing with females. Here we investigate patterns of male interventions and the effect of coalitions and sociality on male fitness in rhesus macaques (Macaca mulatta) with particular focus on male-female interactions. We combined behavioural observations collected on Cayo Santiago with genetic data analysed for male reproductive output and relatedness. Our results revealed that the ten top-ranking males provided the majority of all male support observed. In contrast to other primates, male rhesus macaques mainly formed all-down coalitions suggesting that coalitions are less likely used to enhance male dominance. Males supporting females during and before their likely conception were not more likely to fertilize those females. We also found no evidence that males preferably support their offspring or other close kin. Interestingly, the most important predictor of male support was sociality, since opponents sharing a higher sociality index with a given male were more likely to be supported. Furthermore, a high sociality index of a given male-female dyad resulted in a higher probability of paternity. Overall, our results strengthen the evidence that sociality affects fitness in male primates, but also suggest that in species in which males queue for dominance, it is less likely that males derive fitness benefits from coalitions.
Project description:The majority of carnivore species are described as solitary, but little is known about their social organization and interactions with conspecifics. We investigated the spatial organization and social interactions as well as relatedness of slender mongooses (Galerella sanguinea) living in the southern Kalahari. This is a little studied small carnivore previously described as solitary with anecdotal evidence for male associations. In our study population, mongooses arranged in spatial groups consisting of one to three males and up to four females. Male ranges, based on sleeping sites, were large and overlapping, encompassing the smaller and more exclusive female ranges. Spatial groups could be distinguished by their behaviour, communal denning and home range. Within spatial groups animals communally denned in up to 33% of nights, mainly during winter months, presumably to gain thermoregulatory benefits. Associations of related males gained reproductive benefits likely through increased territorial and female defence. Our study supports slender mongooses to be better described as solitary foragers living in a complex system of spatial groups with amicable social interactions between specific individuals. We suggest that the recognition of underlying 'hidden' complexities in these apparently 'solitary' organizations needs to be accounted for when investigating group living and social behaviour.
Project description:Although both bonobos and chimpanzees are male-philopatric species, outcomes of male-male reproductive competition seem to be more closely associated with mating success in chimpanzees. This suggests that the extent of male reproductive skew is lower in bonobos. In addition, between-group male-male reproductive competition is more lethal in chimpanzees. This suggests that between-group differentiation in male kinship is lower in bonobos. We analysed the paternity of 17 offspring in two bonobo groups and estimated the relatedness of individuals among three neighbouring groups by using DNA extracted from non-invasive samples at Wamba, in the Democratic Republic of the Congo. The alpha males sired at least nine of 17 offspring. This supports a previous finding that the male reproductive skew is higher in bonobos than that in chimpanzees. Average relatedness among males within groups was significantly higher than that among males across groups, whereas there was no significant difference among females between within and across groups. These results are consistent with male philopatry, highly skewed reproductive success of males and female dispersal. Higher average relatedness among males within groups suggest that the differences in hostility towards males of different groups between bonobos and chimpanzees may be explained by factors other than kinship.
Project description:Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard-female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate-guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.
Project description:Kin selection theory predicts that animals should direct costly care where inclusive fitness gains are highest. Individuals may achieve this by directing care at closer relatives, yet evidence for such discrimination in vertebrates is equivocal. We investigated patterns of cooperative care in banded mongooses, where communal litters are raised by adult 'escorts' who form exclusive caring relationships with individual pups. We found no evidence that escorts and pups assort by parentage or relatedness. However, the time males spent escorting increased with increasing relatedness to the other group members, and to the pup they had paired with. Thus, we found no effect of relatedness in partner choice, but (in males) increasing helping effort with relatedness once partner choices had been made. Unexpectedly, the results showed clear assortment by sex, with female carers being more likely to tend to female pups, and male carers to male pups. This sex-specific assortment in helping behaviour has potential lifelong impacts on individual development and may impact the future size and composition of natal groups and dispersing cohorts. Where relatedness between helpers and recipients is already high, individuals may be better off choosing partners using other predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination.
Project description:Sexual dimorphism is typically a result of strong sexual selection on male traits used in male-male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females--but not males--were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela--the primary antagonistic weapon in snapping shrimps--increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female-female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.
Project description:One of the basic tenets of sexual selection is that male reproductive success should be large in polygynous species. Here, we analysed 6 years of molecular genetic data from a semi-free-ranging population of rhesus macaques (Macaca mulatta), using Nonac's B index, to assess the level of male reproductive skew in the study troop. On average, the top sire in each year produced 24% of the infants, while 71% of troop males sired no offspring at all. Consequently, 74% of infants had at least one paternal half-sibling in their own birth cohort. Reproductive success was greatest for high-ranking males, males who spent the whole mating season in the troop and males of 9-11 years of age. Heterozygosity for major histocompatibility complex (MHC) class II gene DQB1 was the strongest single predictor of male reproductive success. A negative relationship suggestive of female mate choice was noted between the B index and the proportion of extragroup paternities. Reproductive skew was not associated with relatedness among potential sires or with female cycle synchrony. We conclude that reproductive skew in male rhesus macaques is best accounted for by the 'limited-control' model, with multiple factors interacting to regulate individual reproductive output.
Project description:Males compete over mating and fertilization, and often harm females in the process. Inclusive fitness theory predicts that increasing relatedness within groups of males may relax competition and discourage male harm of females as males gain indirect benefits. Recent studies in Drosophila melanogaster are consistent with these predictions, and have found that within-group male relatedness increases female fitness, though others have found no effects. Importantly, these studies did not fully disentangle male genetic relatedness from larval familiarity, so the extent to which modulation of harm to females is explained by male familiarity remains unclear. Here we performed a fully factorial design, isolating the effects of male relatedness and larval familiarity on female harm. While we found no differences in male courtship or aggression, there was a significant interaction between male genetic relatedness and familiarity on female reproduction and survival. Relatedness among males increased female lifespan, reproductive lifespan and overall reproductive success, but only when males were familiar. By showing that both male relatedness and larval familiarity are required to modulate female harm, these findings reconcile previous studies, shedding light on the potential role of indirect fitness effects on sexual conflict and the mechanisms underpinning kin recognition in fly populations.
Project description: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.
Project description:Most mammals live in social groups in which members form differentiated social relationships. Individuals may vary in their degree of sociality, and this variation can be associated with differential fitness. In some species, for example, female sociality has a positive effect on infant survival. However, investigations of such cases are still rare, and no previous study has considered how male infanticide might constrain effects of female sociality on infant survival. Infanticide is part of the male reproductive strategy in many mammals, and it has the potential to override, or even reverse, effects of female reproductive strategies, including sociality. Therefore, we investigated the relationships between female sociality, offspring survival, and infanticide risk in wild white-faced capuchin monkeys using long-term data from Santa Rosa, Costa Rica. Female capuchins formed differentiated bonds, and bond strength was predicted by kin relationship, rank difference, and the presence of female infants. Most females formed stable bonds with their top social partners, although bond stability varied considerably. Offspring of highly social females, who were often high-ranking females, exhibited higher survivorship during stable periods compared with offspring of less social females. However, offspring of highly social females were more likely to die or disappear during periods of alpha male replacements, probably because new alpha males are central to the group, and therefore more likely to target the infants of highly social, central females. This study shows that female sociality in mammals can have negative fitness consequences that are imposed by male behavior.