Kin selection, local competition, and reproductive skew

In a spatially structured population, limited dispersal gives rise to local relatedness, potentially favoring indiscriminate helping behavior. However, it also leads to local competition, which reduces the benefits of helping local kin. This tension has become the focus for a growing body of theoretical work. Existing models, however, have focused chiefly on the net impact of limited dispersal on cooperative or competitive effort in a homogeneous population. Here, I extend existing models of kin selection in a group-structured population to allow for asymmetries in expected fecundity and reproductive success among group members. I explore the consequent impact of limited dispersal on the evolution of helping and harming behavior, and on the degree of reproductive inequality or skew. I show that when individuals in a group differ in their expected fecundity, limited dispersal gives rise to kin selection for harming behavior on the part of more fecund individuals, and for helping behavior on the part of less fecund individuals. As a result, philopatry tends to exaggerate differences in reproductive success, and so promotes greater reproductive skew.     

Relatedness and Social Behaviors in <Emphasis Type="Italic">Cercopithecus solatus</Emphasis>

Inclusive fitness and kin selection theories predict that organisms will evolve biased behavior toward kin when the inclusive fitness benefits outweigh the costs of such behaviors. Researchers have long observed that primates bias their behavior toward relatives, particularly maternal kin. We examined the effect of kinship on social behaviors in a semifree-ranging colony of Cercopithecus solatus, a poorly studied forest guenon species. We used microsatellite loci and paternity analyses to determine the degree of relatedness between individuals, as well as kinship. Individuals biased some of their behavior according to relatedness. Specifically, related individuals are more spatially associated and less aggressive toward each other. When we replaced the relatedness coefficients with defined kin categories, Cercopithecus solatus seemed to behave preferentially toward maternal kin versus paternal kin. Even though the setting of the colony and the small sample size limit our conclusions, we discuss the potential implications of our finding for the study of the impact of kin selection in primate social relationships.     

Ground squirrel sociality and the quest for the 'holy grail': does kinship influence behavioral discrimination by juvenile Columbian ground squirrels?

Research on social discrimination by ground-dwelling squirrelshas focused on die ability of squirrels to discriminate kinfrom nonkin. The predominant mechanism underlying that abilityis social familiarization. Although familiarity-based mechanismsmay result in kin discrimination where kin are associated reliablyin space and time, past investigations have largely ignoredadditional levels of social discrimination that may result fromongoing familiarization in the natural context Here we presentdata from a cross-fostering experiment that examines the relativecontributions of rearing association and relatedness to subsequentbehavioral discrimination among juvenile Columbian ground squirrels(Spermophilus columbianus). Rearing association significantlyinfluenced recognitive and agonistic behavior among juvenileswhile relatedness proved insignificant in affecting behavioralinteractions. Thus, direct familiarization in the natal burrowis both sufficient and necessary to account for the transitiveappearance of kin-differential behavior among newly emergedjuveniles documented in previous studies. Reanalyses of datafrom field experiments on S. columbianus social discriminationfail to detect any evidence of kin-biased behavior, and evidencefrom studies purporting to document kinship effects is equivocalat best Taken together with more recent findings, the scantdata suggestive of kin discrimination by Columbian ground squirrelsare best viewed as an artifact of selection promoting the discriminationof familiar from unfamiliar individuals at the level of localizedgroups. Fitness payoffs of such discrimination may accrue viareciprocal altruism, or ‘dear-enemy’ recognition,and would promote the evolution and maintenance of socialitywithout recourse to indirect components of inclusive fitnesscommonly invoked to explain ground squirrel sociality. Finally,our data call into doubt the notion that mechanisms allowingthe direct assessment of kinship should be common among themore social sciurids.     

Social network structure in wintering golden‐crowned sparrows is not correlated with kinship

Stable social organization in a wide variety of organisms has been linked to kinship, which can minimize conflict due to the indirect fitness benefits from cooperating with relatives. In birds, kin selection has been mostly studied in the context of reproduction or in species that are social year round. Many birds however are migratory, and the role of kinship in the winter societies of these species is virtually unexplored. In a previous study, we discovered striking social complexity and stability in a wintering population of migratory golden‐crowned sparrows (Zonotrichia atricapilla) – individuals repeatedly form close associations with the same social partners, including across multiple winters. Here, we test the possibility that kinship might be involved in these close and stable social affiliations. We examine the relationship between kinship and social structure for two of the consecutive wintering seasons from the previous study. We found no evidence that social structure was influenced by kinship. Relatedness between most pairs of individuals was at most that of first cousins (and mostly far lower). Genetic networks based on relatedness do not correspond to the social networks, and Mantel tests revealed no relationship between kinship and pairwise interaction frequency. Kinship also failed to predict social structure in more fine‐grained analyses, including analyses of each sex separately (in the event that sex‐biased migration might limit kin selection to one sex), and separate analyses for each social community. The complex winter societies of golden‐crowned sparrows appear to be based on cooperative benefits unrelated to kin selection.     

Promiscuity drives self-referent kin recognition

Kin selection theory has been one of the most significant advances in our understanding of social behavior . However, the discovery of widespread promiscuity has challenged the evolutionary importance of kin selection because it reduces the benefit associated with helping nestmates . This challenge would be resolved if promiscuous species evolved a self-referent kin-recognition mechanism that enables individuals to differentiate kin and nonkin . Here, we take advantage of an asymmetry in the level of promiscuity among males of alternative life histories in the bluegill sunfish (Lepomis macrochirus). We show that, as a consequence of this asymmetry, offspring of "parental" males have a high level of relatedness to nestmates, whereas offspring of "cuckolder" males have a low level of relatedness to nestmates. We find that offspring of parentals do not use a direct recognition mechanism to discriminate among nestmates, whereas offspring of cuckolders use kin recognition by self-referent phenotype matching to differentiate between kin and nonkin. Furthermore, we estimate that the cost of utilizing such self-referent kin recognition is equivalent to a relatedness (R) of at least 0.06. These results provide compelling evidence for adaptive use of kin recognition by self-referent phenotype matching and confirm the importance of kinship in social behavior.     

Male reproductive skew, paternal relatedness, and female social relationships

Female social relationships among primates are thought to be shaped by socio-ecological factors and phylogenetic constraints. We suggest that patterns of paternal relatedness among females influence measures of social tolerance that have been used to classify species into different social relationship categories. As kin support and kin preference have only been measured for matrilineal kin and related individuals exchange less aggression and have a higher conciliatory tendency, the observed low nepotism levels and high tolerance levels may be an artifact of hidden paternal relatedness among the nonkin category. Using comparative data on macaques, we investigate this hypothesis using male reproductive skew as a proxy for paternal relatedness. Within the limitations of the study we show that populations classified as being less nepotistic, and more tolerant exhibit higher levels of reproductive skew. This first result and the reasoning behind may motivate future students of social relationships to take paternal relatedness into consideration. Potential implications of this finding if repeated with larger samples include that variation in aspects of macaque social relationships may be explained without considering phylogeny or the strength of between-group contest competition for food.     

Estimating relatedness in social groups

Genetic relatedness is a vital parameter in the evolution of social behaviour by kin selection. It can be easily estimated using genetic markers and calculating the genotypic correlation or regression of group members. Spatial gene frequency differentiation, due to population subdivision or isolation by distance, boosts the relatedness estimates. In such cases it may be useful to partition the estimate into components, the operational relatedness is normally that among individuals in social groups within the same subpopulation. Although it is straightforward to estimate the average relatedness in social groups, estimating values for specific individuals with the help of genetic markers is still problematic. Current estimators tend to give biased values and the sampling error is large. In spite of these shortcomings, studies of social behaviour combining relatedness and reproductive success are sorely needed.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco (Ctenomys talarum), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.     

Multiple paternities increase genetic diversity of offspring in Brandt's voles

Mating system and philopatry influence the genetic structure of a social group in mammals. Brandt's vole (Lasiopodomys brandtii) lives in social groups year-round and has male biased dispersal, which makes the vole a model system for studies of genetic consequences of mating system and philopatry. This study aimed to test the hypotheses that: (1) multiple paternity (MP) would exist in Brandt's voles, enhance offspring genetic diversity and reduce genetic relatedness between littermates; (2) promiscuity would occur in this species in that males and females mate with multiple partners; and (3) plural breeders of a social group would be genetically related because of philopatry of female juveniles in Brandt's voles. Paternity analysis indicated that MP occurred in 11 (46%) of 24 social groups examined and that promiscuity existed in this species. Multiple paternity litters had twice the offspring genetic diversity and half the average within-litter genetic relatedness of single paternity litters. We also found plural breeding females in six social groups. Average pairwise genetic relatedness of plural breeders ranged from 0.41 to 0.72 in four social groups, suggesting first-order kinship. Future studies need to investigate effects of reproductive skew and MP on population genetic structure of Brandt's voles.     

Kin Selection in Primate Groups

Altruism poses a problem for evolutionary biologists because natural selection is not expected to favor behaviors that are beneficial to recipients, but costly to actors. The theory of kin selection, first articulated by Hamilton (1964), provides a solution to the problem. Hamilton's well-known rule (br > c) provides a simple algorithm for the evolution of altruism via kin selection. Because kin recognition is a crucial requirement of kin selection, it is important to know whether and how primates can recognize their relatives. While conventional wisdom has been that primates can recognize maternal kin, but not paternal kin, this view is being challenged by new findings. The ability to recognize kin implies that kin selection may shape altruistic behavior in primate groups. I focus on two cases in which kin selection is tightly woven into the fabric of social life. For female baboons, macaques, and vervets maternal kinship is an important axis of social networks, coalitionary activity, and dominance relationships. Detailed studies of the patterning of altruistic interactions within these species illustrate the extent and limits of nepotism in their social lives. Carefully integrated analyses of behavior, demography, and genetics among red howlers provide an independent example of how kin selection shapes social organization and behavior. In red howlers, kin bonds shape the life histories and reproductive performance of both males and female. The two cases demonstrate that kin selection can be a powerful source of altruistic activity within primate groups. However, to fully assess the role of kin selection in primate groups, we need more information about the effects of kinship on the patterning of behavior across the Primates and accurate information about paternal kin relationships.     

Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal

Hamilton demonstrated that the evolution of cooperative behaviour is favoured by high relatedness, which can arise through kin discrimination or limited dispersal (population viscosity). These two processes are likely to operate with limited overlap: kin discrimination is beneficial when variation in relatedness is higher, whereas limited dispersal results in less variable and higher average relatedness, reducing selection for kin discrimination. However, most empirical work on eukaryotes has focused on kin discrimination. To address this bias, we analysed how kin discrimination and limited dispersal interact to shape helping behaviour across cooperatively breeding vertebrates. We show that kin discrimination is greater in species where the: (i) average relatedness in groups is lower and more variable; (ii) effect of helpers on breeders reproductive success is greater; and (iii) probability of helping was measured, rather than the amount of help provided. There was also an interaction between these effects with the correlation between the benefits of helping and kin discrimination being stronger in species with higher variance in relatedness. Overall, our results suggest that kin discrimination provides a route to indirect benefits when relatedness is too variable within groups to favour indiscriminate cooperation.     

Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus

Populations of red grouse ( Lagopus lagopus scoticus ) undergo regular multiannual cycles in abundance. The 'kinship hypothesis' posits that such cycles are caused by changes in kin structure among territorial males producing delayed density-dependent changes in aggressiveness, which in turn influence recruitment and regulate density. The kinship hypothesis makes several specific predictions about the levels of kinship, aggressiveness and recruitment through a population cycle: (i) kin structure will build up during the increase phase of a cycle, but break down prior to peak density; (ii) kin structure influences aggressiveness, such that there will be a negative relationship between kinship and aggressiveness over the years; (iii) as aggressiveness regulates recruitment and density, there will be a negative relationship between aggressiveness in one year and both recruitment and density in the next; (iv) as kin structure influences recruitment via an affect on aggressiveness, there will be a positive relationship between kinship in one year and recruitment the next. Here we test these predictions through the course of an 8-year cycle in a natural population of red grouse in northeast Scotland, using microsatellite DNA markers to resolve changing patterns of kin structure, and supra-orbital comb height of grouse as an index of aggressiveness. Both kin structure and aggressiveness were dynamic through the course of the cycle, and changing patterns were entirely consistent with the expectations of the kinship hypothesis. Results are discussed in relation to potential drivers of population regulation and implications of dynamic kin structure for population genetics.     

Kin recognition in social bees

Kin recognition in social insects has become a central issue in sociobiology because studies of the recognition abilities of social insects provide a test of kin selection theory. W.D. Hamilton(1) formalized kin selection theory by showing how individuals can gain fitness by increasing the reproductive output of relatives (kin). The social interactions of individuals, or groups, should be influenced by the genetic structure of the population. The ability to recognize kin can increase the adaptive value of social behavior by modulating it according to genetic relationship. From this, the specific prediction emerges: if individuals can distinguish among others with which they interact on the basis of the degree to which they are related, then behavior should be biased preferentially toward more closely related reproductive individuals.     

Fitness consequences of spousal relatedness in 46 small-scale societies

Social norms that regulate reproductive and marital decisions generate impressive cross-cultural variation in the prevalence of kin marriages. In some societies, marriages among kin are the norm and this inbreeding creates intensive kinship networks concentrated within communities. In others, especially forager societies, most marriages are between more genealogically and geographically distant individuals, which generates a larger number of kin and affines of lesser relatedness in more extensive kinship networks spread out over multiple communities. Here, we investigate the fitness consequence of kin marriages across a sample of 46 small-scale societies (12 439 marriages). Results show that some non-forager societies (including horticulturalists, agriculturalists and pastoralists), but not foragers, have intensive kinship societies where fitness outcomes (measured as the number of surviving children in genealogies) peak at commonly high levels of spousal relatedness. By contrast, the extensive kinship systems of foragers have worse fitness outcomes at high levels of spousal relatedness. Overall, societies with greater levels of inbreeding showed a more positive relationship between fitness and spousal relatedness.     

Colony sex ratios vary with queen number but not relatedness asymmetry in the ant Formica exsecta

Split-sex-ratio theory assumes that conflict over whether to produce predominately males or female reproductives (gynes) is won by the workers in haplodiploid insect societies and the outcome is determined by colony kin structure. Tests of the theory have the potential to provide support for kin-selection theory and evidence of social conflict. We use natural variation in kinship among polygynous (multiple-queen) colonies of the ant Formica exsecta to study the associations between sex ratios and the relatedness of workers to female versus male brood (relatedness asymmetry). The population showed split sex ratios with about 89% of the colonies producing only males, resulting in an extremely male-biased investment ratio in the population. We make two important points with our data. First, we show that queen number may affect sex ratio independently of relatedness asymmetry. Colonies producing only males had greater genetic effective queen number but did not have greater relatedness asymmetry from the perspective of the adult workers that rear the brood. This lack of a difference in relatedness asymmetry between colonies producing females and those producing only males was associated with a generally low relatedness between workers and brood. Second, studies that suggest support for the relatedness-asymmetry hypothesis based on indirect measures of relatedness asymmetry (e.g. queen number estimated from relatedness data taken from the brood only) should be considered with caution. We propose a new hypothesis that explains split sex ratios in polygynous social insects based on the value of producing replacement queens.     

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called 'clans', resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group-mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group-mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon-like sociality among top-level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio-ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species' range, and describe the long-term fitness consequences of rank-related variation in resource access among clan-mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non-kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year-round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.     

Relatedness and genetic structure in a socially polymorphic population of the spider Anelosimus studiosus

The evolution of sociality remains a challenge in evolutionary biology and a central question is whether association between kin is a critical factor favouring the evolution of cooperation. This study examines genetic structure of Anelosimus studiosus, a spider exhibiting polymorphic social behaviour. Two phenotypes have been identified: an ‘asocial’ phenotype with solitary female nests and a ‘social’ phenotype with multi‐female/communal nests. To address the questions of whether these phenotypes are differentiated populations and whether cooperative individuals are closely related, we used microsatellites to analyse individuals from both communal and solitary nests. We found no evidence of differentiation between social and solitary samples, implying high rates of interbreeding. This is consistent with the hypothesis that these phenotypes coexist as a behavioural polymorphism within populations. Pairwise relatedness coefficients were used to test whether cooperating individuals are more closely related than expected by chance. Pairwise relatedness of females sharing communal webs averaged 0.25, the level expected for half‐siblings and significantly more closely related than random pairs from the population. Solitary females collected at similar distances to the communal spider pairs were also more closely related than expected by chance (mean relatedness = 0.18), but less related than social pairs. These results imply that low dispersal contributes to increase likelihood of interaction between kin, but relatedness between social pairs is not explained by spatial structure alone. We propose that these phenotypes represent stages in the evolution of sociality, where viscous population structure creates opportunities for kin selection and cooperation is favoured under certain environmental conditions.     

Relatedness does not predict vigilance in a population of the social rodent Octodon degus

The possibility that social foragers adjust and coordinate their scanning activity when in the presence of close relatives to attain inclusive fitness benefits remains controversial and scarcely examined. To this aim, we first tested the null hypothesis of no association between foraging individuals of the diurnal rodent, Octodon degus and their pairwise relatedness (six microsatellite loci), under natural conditions. Secondly, we examined the influence of relatedness on scan effort (percent overlapping) and temporal distribution of scanning using linear regression. Finally, we evaluated whether temporal distributions of scanning were significantly lower (coordination) or higher (synchrony) than random expectations using bootstrapping. We found that pairwise relatedness between focal degus and their foraging partner did not influence the scan effort or the temporal distribution of scanning. These original, field-based findings imply that vigilance behavior in socially foraging degus is unlikely to be kin-selected and adds to results from previous lab studies in that kinship remains a poor predictor of social behavior in these animals. Overall, our study adds to others revealing that kin selection may not have had an impact on aspects of social behavior such as vigilance during social foraging.     

Kin selection and the evolution of virulence

Social interactions between conspecific parasites are partly dependent on the relatedness of interacting parasites (kin selection), which, in turn, is predicted to affect the extent of damage they cause their hosts (virulence). High relatedness is generally assumed to favour less competitive interactions, but the relationship between relatedness and virulence is crucially dependent on the social behaviour in question. Here, we discuss the rather limited body of experimental work that addresses how kin-selected social behaviours affect virulence. First, if prudent use of host resources (a form of cooperation) maximizes the transmission success of the parasite population, decreased relatedness is predicted to result in increased host exploitation and virulence. Experimental support for this well-established theoretical result is surprisingly limited. Second, if parasite within-host growth rate is a positive function of cooperation (that is, when individuals need to donate public goods, such as extracellular enzymes), virulence is predicted to increase with increasing relatedness. The limited studies testing this hypothesis are broadly consistent with this prediction. Finally, there is some empirical evidence supporting theory that suggests that spiteful behaviours are maximized at intermediate degrees of relatedness, which, in turn, leads to minimal virulence because of the reduced growth rate of the infecting population. We highlight the need for further thorough experimentation on the role of kin selection in the evolution of virulence and identify additional biological complexities to these simple frameworks.