Inclusive fitness of 'kissing cousins': new evidence of a role for kin selection in the evolution of extra-pair mating in birds

Social monogamy is nearly ubiquitous across avian taxa,but evidence from a proliferation of studies utilizing molecular paternity analysis suggests that sexual monogamy is the rare exception rather than the rule (Griffith et al. 2002). Efforts to explain the prevalence of extra-pair paternity (EPP) have largely focused on the potential fitness benefits for offspring genetic quality, as females are less likely to benefit directly from seeking extra-pair mates. In particular, there has been considerable interest in the degree to which EPP may represent an adaptive female strategy to avoid inbreeding (or outbreeding)depression when paired with a highly related (or unrelated)social mate (Kempenaers 2007). Others have argued that, because relatives share many genes identical by descent,females might increase their own inclusive fitness by providing additional breeding opportunities to genetically related males (Waser et al. 1986; Kokko & Ots 2006). Thus, in the absence of significant inbreeding depression, pursuing EPP with relatives should be favoured by kin selection, although there exist few unambiguous empirical examples of such preferences in the literature. In this issue of Molecular Ecology, Wang &Lu (2011) present an analysis of mating patterns with respect to genetic relatedness of social and extra-pair partners in the ground tit (Parus humilis), a facultative cooperative breeder in which socially monogamous pairs occasionally form cooperative groups with unpaired helper males (Fig. 1). Consistent with the predictions of the kin-selection hypothesis, females in both bi-parental and cooperative groups preferentially engaged in extra-pair matings with relatives, irrespective of relatedness to their social mates, and while suffering no apparent costs of inbreeding depression in their progeny. These finding shave several exciting implications for our understanding of avian mating system diversity and the evolution of cooperative breeding.     

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

Genetic structure, relatedness and helping behaviour in the yellow mongoose in a farmland and a natural habitat

The yellow mongoose Cynictis penicillata is a facultatively social species and provides an opportunity to study the evolution of social behaviour. We examined genetic structure, relatedness and helping behaviour in the yellow mongoose in natural habitat in the Kalahari Desert, where the species lives in small family groups of up to four individuals and shows no cooperative breeding; and in farmland in the Western Cape Province of South Africa, where they live in larger groups of up to 13 individuals, engage in numerous social interactions and show cooperative breeding. The farmland population showed significant inbreeding, and lower genetic variability than the desert population, but there was no evidence of a recent population bottleneck. The genetic relatedness between individuals within social groups and that between future potential helpers and pups were higher in the farmland population than in the desert population. However, based on a limited sample, helping effort (in the farmland population) was not preferentially directed towards kin. Thus, the origin of helping in the farmland population is consistent with kin selection, but in the absence of kin discrimination, future research should investigate whether long-term breeding opportunities or group augmentation contribute to maintaining cooperative breeding in this population.     

Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin

Kin selection predicts that helpers in cooperative systems should preferentially aid relatives to maximize fitness. In family-based groups, this can be accomplished simply by assisting all group members. In more complex societies, where large numbers of kin and non-kin regularly interact, more sophisticated kin-recognition mechanisms are needed. Bell miners (Manorina melanophrys) are just such a system where individuals regularly interact with both kin and non-kin within large colonies. Despite this complexity, individual helpers of both sexes facultatively work harder when provisioning the young of closer genetic relatedness. We investigated the mechanism by which such adaptive discrimination occurs by assessing genetic kinship influences on the structure of more than 1900 provisioning vocalizations of 185 miners. These 'mew' calls showed a significant, positive linear increase in call similarity with increasing genetic relatedness, most especially in comparisons between male helpers and the breeding male. Furthermore, individual helping effort was more heavily influenced by call similarity to breeding males than to genetic relatedness, as predicted if call similarity is indeed the rule-of-thumb used to discriminate kin in this system. Individual mew call structure appeared to be inflexible and innate, providing an effective mechanism by which helpers can assess their relatedness to any individual. This provides, to our knowledge, the first example of a mechanism for fine-scale kin discrimination in a complex avian society.     

Mother's little helpers: What we know (and don't know) about cooperative infant care in callitrichines

Since Darwin ( 1859 ), scientists have been puzzled by how behaviors that impose fitness costs on helpers while benefiting their competitors could evolve through natural selection. Hamilton's ( 1964 ) theory of inclusive fitness provided an explanation by showing how cooperative behaviors could be adaptive if directed at closely related kin. Recent studies, however, have begun to question whether kin selection is sufficient to explain cooperative behavior in some species (Bergmüller, Johnstone, Russell, & Bshary, 2007 ). Many researchers have instead emphasized the importance of direct fitness benefits for helpers in the evolution of cooperative breeding systems. Furthermore, individuals can vary in who, when, and how much they help, and the factors that affect this variation are poorly understood (Cockburn, 1998 ; Heinsohn, 2004 ). Cooperative breeders thus provide excellent models for the study of evolutionary theories of cooperation and conflict (Cant, 2012 ).     

A theoretical basis for measures of kin selection in subdivided populations: finite populations and localized dispersal

The analysis of kin selection in subdivided populations has been hampered by the lack of well‐defined measures of genealogical relatedness in the presence of localized dispersal. Furthermore, the usual arguments underlying the definition of game‐theoretical measures of inclusive fitness are not exact under localized dispersal. We define such measures to give the first‐order effects of selection on the probability of fixation of an allele. The derived measures of kin selection and relatedness are valid in finite populations and under localized dispersal. For the infinite island model, the resulting measure of kin selection is equivalent to a previously used measure. In other cases its definition is based on definitions of relatedness which are different from the usual ones. To illustrate the approach, we reanalyse a model with localized dispersal. We consider sex ratio evolution under sex‐specific dispersal behaviour, and the results confirm the earlier conclusion that the sex ratio is biased towards the sex with the dispersal rate closer to the optimal dispersal rate in the absence of sex‐specific dispersal behaviour.     

Complex social organization reflects genetic structure and relatedness in the cooperatively breeding bell miner, Manorina melanophrys

The cooperatively breeding bell miner, Manorina melanophrys, differs from most other cooperative breeding species in the complexity of its social system, where discrete social organization occurs on at least three levels. Microsatellite markers were used to investigate the degree of genetic structure underlying the social organization of M. melanophrys by comparing colonies, coteries and nest contingents. The genetic data confirmed behavioural observations of M. melanophrys living in male kin-based groups between which females disperse short distances to breed. Estimates of FST revealed restricted gene flow between eight colonies located within 30 km that was significantly associated with geographical distance when the two most distant colonies were included. Within a high density colony significant differences were found between coteries; analysis of the degree of relatedness between coterie members showed that this is due to related individuals associating preferentially with each other. Similarly, the contingent of individuals attending a nest were generally close relatives of the young they were aiding, supporting models invoking kin selection as the selective agency mediating helping.     

Pup escorting in the communal breeding banded mongoose: behavior, benefits, and maintenance

In cooperatively breeding species, helpers typically providefood to offspring, and distribute food throughout the broodor litter. However, in the communal breeding banded mongoose(Mungos mungo), some group members escort individual pups duringtheir period of dependence, and escorts consistently associatewith the same pup, although not all pups have an escort. Theaim of the present study was to determine whether group membersactively care for pups, pups benefit from association, and escortsor pups maintain association. Adult banded mongooses provision,protect, carry, groom, and play with pups. Although escortsfed pups more than did nonescorts, escorted pups were neitherlarger nor in better condition than were nonescorted pups atthe end of the association period. Nevertheless, escorted pupswere more likely to survive the association period than werenonescorted pups, providing evidence that carers confer beneficialeffects on their recipients. However, the recipients are unlikelyto be the genetic offspring of the escort because it is thepup that maintains the pup-escort association, and escorts,rather than showing a preference for provisioning their pairedpup, follow a "feed the closest pup" rule. Although carers gainindirect fitness benefits through increasing survival of relatedpups, the lack of kin discrimination means carers are unableto maximize their fitness by preferentially escorting theirown offspring or the offspring of closer relatives.     

Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers

Abstract.— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis . A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.     

Offspring retention in the Siberian jay {Perisoreus infaustus): the prolonged brood care hypothesis

We examined aggressive behavior in Siberian jay groups containingboth retained offspring and immigrant juveniles during winterfeeding and during breeding. Selective tolerance of retainedoffspring by parental birds in winter suggests that cooperationevolved through kin selection. Parents exhibited a self-restraintin aggression towards retained offspring at food in winter.Comparatively, nonkin immigrants were aggressively preventedfrom sharing food by the local pair. Parental tolerance in wintercould bring inclusive fitness gains through the direct kin componentif retained offspring experience relaxed competition and enhancedsurvival. Parental tolerance would then favor the evolutionof delayed dispersal. There is no evidence that delayed dispersalamong Siberian jays should have evolved because of indirectfitness benefits to retained offspring from helping to raiseyounger siblings. Offspring retained by parents did not participatein incubation, feeding or nest defense.     

A comparison of techniques for assessing dispersal behaviour in gundis: revealing dispersal patterns in the absence of observed dispersal behaviour

Knowledge of the dispersal status of group members is important to understanding how sociality may have evolved within a species. I assessed the effectiveness of four techniques for elucidating dispersal behaviour in a rock-dwelling rodent ( Ctenodactylus gundi ) with small group sizes (2–10 animals): genetic parentage assignment, haplotype data and kinship analyses, assignment testing, and F -statistics. The first two methods provided the greatest insight into gundi dispersal behaviour. Assignment testing and F -statistics proved of limited use for elucidating fine-scale dispersal, but could detect large-scale patterns despite low sex-biased dispersal intensity (1.9 : 1) because of moderate genetic differentiation among groups ( F _ST = 0.10). Findings are discussed in light of current dispersal theory. In general, gundi dispersal is plastic, and seems to be dependent on body weight (for males), group composition, and scale of analysis (total dispersal events recorded within the population were almost twice the immigration rate into the population). Most groups were comprised of a single matriline and one immigrant male. Immigrant rather than philopatric males bred with group females. Dispersal among groups was male-biased, but dispersal or philopatry could occur by either sex. During a drought, both sexes delayed dispersal and cooperative social units formed. Whether such behaviour resulted directly from the drought or not remains unclear, however, since comparative information was not available from nondrought years. Combining fine-scale analyses with information on large-scale patterns provided substantial insight into gundi dispersal behaviour despite the limited movement of animals during a drought, and may prove useful for elucidating dispersal behaviour in other social animals.     

Hamilton's rule and the causes of social evolution

Hamilton''s rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton''s rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton''s rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton''s rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton''s rule regarding conditions for social evolution and their causes.     

Cumulative cultural dynamics and the coevolution of cultural innovation and transmission: an ESS model for panmictic and structured populations

When individuals in a population can acquire traits through learning, each individual may express a certain number of distinct cultural traits. These traits may have been either invented by the individual himself or acquired from others in the population. Here, we develop a game theoretic model for the accumulation of cultural traits through individual and social learning. We explore how the rates of innovation, decay, and transmission of cultural traits affect the evolutionary stable (ES) levels of individual and social learning and the number of cultural traits expressed by an individual when cultural dynamics are at a steady‐state. We explore the evolution of these phenotypes in both panmictic and structured population settings. Our results suggest that in panmictic populations, the ES level of learning and number of traits tend to be independent of the social transmission rate of cultural traits and is mainly affected by the innovation and decay rates. By contrast, in structured populations, where interactions occur between relatives, the ES level of learning and the number of traits per individual can be increased (relative to the panmictic case) and may then markedly depend on the transmission rate of cultural traits. This suggests that kin selection may be one additional solution to Rogers's paradox of nonadaptive culture.     

Where sociality and relatedness diverge: the genetic basis for hierarchical social organization in African elephants

Hierarchical properties characterize elephant fission–fusion social organization whereby stable groups of individuals coalesce into higher order groups or split in a predictable manner. This hierarchical complexity is rare among animals and, as such, an examination of the factors driving its emergence offers unique insight into the evolution of social behaviour. Investigation of the genetic basis for such social affiliation demonstrates that while the majority of core social groups (second-tier affiliates) are significantly related, this is not exclusively the case. As such, direct benefits received through membership of these groups appear to be salient to their formation and maintenance. Further analysis revealed that the majority of groups in the two higher social echelons (third and fourth tiers) are typically not significantly related. The majority of third-tier members are matrilocal, carrying the same mtDNA control region haplotype, while matrilocality among fourth-tier groups was slightly less than expected at random. Comparison of results to those from a less disturbed population suggests that human depredation, leading to social disruption, altered the genetic underpinning of social relations in the study population. These results suggest that inclusive fitness benefits may crystallize elephant hierarchical social structuring along genetic lines when populations are undisturbed. However, indirect benefits are not critical to the formation and maintenance of second-, third- or fourth-tier level bonds, indicating the importance of direct benefits in the emergence of complex, hierarchical social relations among elephants. Future directions and conservation implications are discussed.     

Social genetic and social environment effects on parental and helper care in a cooperatively breeding bird

Phenotypes expressed in a social context are not only a function of the individual, but can also be shaped by the phenotypes of social partners. These social effects may play a major role in the evolution of cooperative breeding if social partners differ in the quality of care they provide and if individual carers adjust their effort in relation to that of other carers. When applying social effects models to wild study systems, it is also important to explore sources of individual plasticity that could masquerade as social effects. We studied offspring provisioning rates of parents and helpers in a wild population of long-tailed tits Aegithalos caudatus using a quantitative genetic framework to identify these social effects and partition them into genetic, permanent environment and current environment components. Controlling for other effects, individuals were consistent in their provisioning effort at a given nest, but adjusted their effort based on who was in their social group, indicating the presence of social effects. However, these social effects differed between years and social contexts, indicating a current environment effect, rather than indicating a genetic or permanent environment effect. While this study reveals the importance of examining environmental and genetic sources of social effects, the framework we present is entirely general, enabling a greater understanding of potentially important social effects within any ecological population.