Kin selection and the evolution of sexual conflict

Males and females do not always share the same evolutionary interests. This is particularly true in the case of multiple mating, where male–male competition can often lead to adaptations that are harmful to the female, and females can evolve counter adaptations to reduce the benefits males gain from such traits. Although social evolution has made substantial progress from kin selection theory, most studies of sexual conflict have ignored the effects of genetic relatedness. Here, I use a model of male harm and female resistance to investigate how kin selection affects the evolution of sexual conflict. Building on models of social evolution, I show that relatedness inhibits sexual conflict, in terms of male harm, whereas it has no effect on the evolution female resistance. This study examines a previously neglected mechanism that can potentially help to resolve sexual conflict over mating and highlights the potential importance of considering relatedness in empirical studies of sexual conflict.     

Limited food induces nepotism in drywood termites

The evolution of cooperation and altruistic behaviour where individuals forego their own reproduction to help others reproduce can be explained by kin selection. Depending on the costs and benefits provided, altruism can be evolutionarily favoured if it is directed at close relatives. A considerable body of data supports the role of relatedness as a key determinant of cooperation and conflict within societies. However, the role of ecological factors and, in particular, how these costs and benefits interact with relatedness remains poorly understood. By studying 16 colonies, here I show that in a drywood termite ecological factors determine the importance of relatedness. In colonies with limited food supply, nestmates restrict cooperative interactions mainly to close relatives, while non-discriminative cooperation occurs when food is abundant. This shows for the first time directly the interaction between ecological conditions and relatedness in shaping cooperation.     

INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS. III. SOCIAL EVOLUTION

Interactions among conspecifics influence social evolution through two distinct but intimately related paths. First, they provide the opportunity for indirect genetic effects (IGEs), where genes expressed in one individual influence the expression of traits in others. Second, interactions can generate social selection when traits expressed in one individual influence the fitness of others. Here, we present a quantitative genetic model of multivariate trait evolution that integrates the effects of both IGEs and social selection, which have previously been modeled independently. We show that social selection affects evolutionary change whenever the breeding value of one individual covaries with the phenotype of its social partners. This covariance can be created by both relatedness and IGEs, which are shown to have parallel roles in determining evolutionary response. We show that social selection is central to the estimation of inclusive fitness and derive a version of Hamilton's rule showing the symmetrical effects of relatedness and IGEs on the evolution of altruism. We illustrate the utility of our approach using altruism, greenbeards, aggression, and weapons as examples. Our model provides a general predictive equation for the evolution of social phenotypes that encompasses specific cases such as kin selection and reciprocity. The parameters can be measured empirically, and we emphasize the importance of considering both IGEs and social selection, in addition to relatedness, when testing hypotheses about social evolution.     

The kin structure of sexual interactions

The origin of sexual reproduction involved the evolution of zygotes from separate genomes and, like other social processes, should therefore be amenable to analysis using kin selection theory. I consider how kin structure affects sexual interactions in three contexts—the evolution of sexual reproduction, sex allocation and sexual conflict. Kin structure helps explain the even-handed replication of paternal and maternal genes under outbreeding. Under inbreeding, it predicts altruistic failure to replicate by one half of the diploid genome. Kin structure predicts optimal sex ratios and potential conflicts over sex ratio within social groups and individuals. Sexual conflict predictably occurs as a function of (i) the probability that current sexual partners will reproduce together in future and (ii) between-partner relatedness. I conclude that systematically analysing the kin structure of sexual interactions helps illuminate their evolution.     

The concurrent evolution of cooperation and the population structures that support it

The evolution of cooperation often depends upon population structure, yet nearly all models of cooperation implicitly assume that this structure remains static. This is a simplifying assumption, because most organisms possess genetic traits that affect their population structure to some degree. These traits, such as a group size preference, affect the relatedness of interacting individuals and hence the opportunity for kin or group selection. We argue that models that do not explicitly consider their evolution cannot provide a satisfactory account of the origin of cooperation, because they cannot explain how the prerequisite population structures arise. Here, we consider the concurrent evolution of genetic traits that affect population structure, with those that affect social behavior. We show that not only does population structure drive social evolution, as in previous models, but that the opportunity for cooperation can in turn drive the creation of population structures that support it. This occurs through the generation of linkage disequilibrium between socio-behavioral and population-structuring traits, such that direct kin selection on social behavior creates indirect selection pressure on population structure. We illustrate our argument with a model of the concurrent evolution of group size preference and social behavior.     

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.     

Kin structure provides no explanation for intruders in social aphids

Nontraditional social organisms have received increasing attention in recent years, because they present opportunities to study the convergent properties of social evolution. Some aphid species are social, occurring in dense clones with specialized morphs that attack predators and parasites. Little is known about how social aphid colonies resolve conflicts of interest when clonal barriers break down. Pemphigus obesinymphae is a North American gall-forming social aphid that produces both nymphal defenders that protect natal clones, and specialized intruders that invade other nearby clones on their host plants. We tested the hypothesis that clones are arranged on their host plants in spatial clusters of related family groups, such that intruders would be biased towards movement within kin groups. Movement within and not between kin groups would then provide insight into the nature of conflict in this social aphid. We sampled eight sites in the eastern United States and in Arizona, and used eight microsatellite markers to estimate pairwise relatedness between spatial groups. We found little evidence of deviation from random distributions of genotypes on their host plants. Evidently, Pem. obesinymphae intruders typically exploit unrelated clones, and spatial orientation provides no solution to the problem of 'polyclonality' in this species. We discuss implications of this result for our understanding of cooperation and conflict in social aphids.     

Genetic relatedness in groups of the humbug damselfish Dascyllus aruanus: small, similar-sized individuals may be close kin

Kin selection plays an important role in the evolution of social behaviour in terrestrial systems. The extent to which kin selection influences the evolution of social behaviour in marine systems is largely unexplored. Generally, it is considered that kin selection is irrelevant in marine systems, because it is assumed that the dispersing larval phase of marine organisms will break up kin associations. Here, we challenge this assumption and investigate the opportunity for kin selection in a coral reef fish: the humbug damselfish Dascyllus aruanus . This fish lives in groups composed of a large male and a number of smaller females and nonbreeders. We use 10 polymorphic microsatellite loci to assess the relatedness of 265 individuals from 35 groups. The mean coefficient of relatedness among group members is 0.01 ± 0.04, suggesting that individuals are not associated with close relatives. However, the distribution of pairwise relatedness of individuals within groups has an overabundance of positive values, and indicates that there might be 35 pairs of close relatives within groups. Further analyses reveal that close relatives likely are similar in size and small in size, suggesting that they might have recruited together. We conclude that it is possible for kin selection to operate in D. aruanus , but kin recognition will be a prerequisite for such selection. This study reveals that individuals can be associated with close relatives, and there is a hidden potential for kin selection, during certain parts of the life cycle of coral reef fishes.     

Kin association during brood care in a facultatively social bird: active discrimination or by‐product of partner choice and demography?

Intra-group relatedness does not necessarily imply kin selection, a leading explanation for social evolution. An overlooked mechanism for generating population genetic structure is variation in longevity and fecundity, referred to as individual quality, affecting kin structure and the potential for cooperation. Individual quality also affects choosiness in partner choice, a key process explaining cooperation through direct fitness benefits. Reproductive skew theory predicts that relatedness decreases with increasing group size, but this relationship could also arise because of quality-dependent demography and partner choice, without active kin association. We addressed whether brood-rearing eider (Somateria mollissima) females preferentially associated with kin using a 6-year data set with individuals genotyped at 19 microsatellite loci and tested whether relatedness decreased with increasing female group size. We also determined the relationship between local relatedness and indices of female age and body condition. We further examined whether the level of female intracoalition relatedness differed from background relatedness in any year. As predicted, median female intra-group relatedness decreased with increasing female group size. However, the proportion of related individuals increased with advancing female age, and older females prefer smaller brood-rearing coalitions, potentially producing a negative relationship between group size and relatedness. There were considerable annual fluctuations in the level of relatedness between coalition-forming females, and in 1year this level exceeded that expected by random association. Thus, both passive and active mechanisms govern kin associations in brood-rearing eiders. Eiders apparently can discriminate between kin, but the benefits of doing so may vary over time.     

Kin selection may inhibit the evolution of reciprocation

Kin selection and reciprocal cooperation provide two candidate explanations for the evolution of cooperation. Models of the evolution of cooperation have typically focussed on one or the other mechanism, despite claims that kin selection could pave the way for the evolution of reciprocal cooperation. We describe a computer simulation model that explicitly supports both kin selection and reciprocal cooperation. The model simulates a viscous population of discrete individuals with social interaction taking the form of the Prisoner's Dilemma and selection acting on performance in these interactions. We recount how the analytical and empirical study of this model led to the conclusion that kin selection may actually inhibit the evolution of effective strategies for establishing reciprocal cooperation.     

Family feuds: social competition and sexual conflict in complex societies

Darwin was initially puzzled by the processes that led to ornamentation in males-what he termed sexual selection-and those that led to extreme cooperation and altruism in complex animal societies-what was later termed kin selection. Here, I explore the relationships between sexual and kin selection theory by examining how social competition for reproductive opportunities-particularly in females-and sexual conflict over mating partners are inherent and critical parts of complex altruistic societies. I argue that (i) patterns of reproductive sharing within complex societies can drive levels of social competition and reproductive conflict not only in males but also in females living in social groups, and ultimately the evolution of female traits such as ornaments and armaments; (ii) mating conflict over female choice of sexual partners can influence kin structure within groups and drive the evolution of complex societies; and (iii) patterns of reproductive sharing and conflict among females may also drive the evolution of complex societies by influencing kin structure within groups. Ultimately, complex societies exhibiting altruistic behaviour appear to have only arisen in taxa where social competition over reproductive opportunities and sexual conflict over mating partners were low. Once such societies evolved, there were important selective feedbacks on traits used to regulate and mediate intra-sexual competition over reproductive opportunities, particularly in females.     

Kinship affects investment by helpers in a cooperatively breeding bird

Helping behaviour in cooperative breeding systems has been attributed to kin selection, but the relative roles of direct and indirect fitness benefits in the evolution of such systems remain a matter of debate. In theory, helpers could maximize the indirect fitness benefits of cooperation by investing more in broods with whom they are more closely related, but there is little evidence for such fine-scale adjustment in helper effort among cooperative vertebrates. In this study, we used the unusual cooperative breeding system of the long-tailed tit Aegithalos caudatus to test the hypothesis that the provisioning effort of helpers was positively correlated with their kinship to broods. We first use pedigrees and microsatellite genotypes to characterize the relatedness between helpers and breeders from a 14 year field study. We used both pedigree and genetic approaches because long-tailed tits have access to pedigree information acquired through social relationships, but any fitness consequences will be determined by genetic relatedness. We then show using both pedigrees and genetic relatedness estimates that alloparental investment by helpers increases as their relatedness to the recipients of their care increases. We conclude that kin selection has played a critical role in moulding the investment decisions of helpers in this cooperatively breeding species.     

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.     

Does kin selection moderate sexual conflict in Drosophila?

Two recent studies provide provocative experimental findings about the potential influence of kin recognition and cooperation on the level of sexual conflict in Drosophila melanogaster. In both studies, male fruit flies apparently curbed their mate-harming behaviours in the presence of a few familiar or related males, suggesting some form of cooperation mediated by kin selection. In one study, the reduction in agonistic behaviour by brothers apparently rendered them vulnerable to dramatic loss of paternity share when competing with an unrelated male. If these results are robust and generalizable, fruit flies could be a major new focus for the experimental study of kin selection and social evolution. In our opinion, however, the restrictive conditions required for male cooperation to be adaptive in this species make it unlikely to evolve. We investigated these phenomena in two different populations of D. melanogaster using protocols very similar to those in the two previous studies. Our experiments show no evidence for a reduction in mate harm based upon either relatedness or familiarity between males, and no reduction in male reproductive success when two brothers are in the presence of an unfamiliar, unrelated, ‘foreign’ male. Thus, the reduction of sexual conflict owing to male cooperation does not appear to be a general feature of the species, at least under domestication, and these contrasting results call for further investigation: in new populations, in the field and in the laboratory populations in which these phenomena have been reported.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Evolution of helping and harming in heterogeneous populations

There has been much interest in understanding how demographic factors can mediate social evolution in viscous populations. Here, we examine the impact of heterogeneity in patch quality--that is, the availability of reproductive resources for each breeder--upon the evolution of helping and harming behaviors. We find that, owing to a cancellation of relatedness and kin competition effects, the evolution of obligate and facultative helping and harming is not influenced by the degree of viscosity in populations characterized by either spatial or temporal heterogeneity in patch quality. However, facultative helping and harming may be favored when there is both spatial and temporal heterogeneity in patch quality, with helping and harming being favored in both high-quality and low-quality patches. We highlight the prospect for using kin selection theory to explain within-population variation in social behavior, and point to the need for further theoretical and empirical investigation of this topic.     

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.     

Adaptive responses and disruptive effects: how major wildfire influences kinship-based social interactions in a forest marsupial

Environmental disturbance is predicted to play a key role in the evolution of animal social behaviour. This is because disturbance affects key factors underlying social systems, such as demography, resource availability and genetic structure. However, because natural disturbances are unpredictable there is little information on their effects on social behaviour in wild populations. Here, we investigated how a major wildfire affected cooperation (sharing of hollow trees) by a hollow-dependent marsupial. We based two alternative social predictions on the impacts of fire on population density, genetic structure and resources. We predicted an adaptive social response from previous work showing that kin selection in den-sharing develops as competition for den resources increases. Thus, kin selection should occur in burnt areas because the fire caused loss of the majority of hollow-bearing trees, but no detectable mortality. Alternatively, fire may have a disruptive social effect, whereby postfire home range-shifts 'neutralize' fine-scale genetic structure, thereby removing opportunities for kin selection between neighbours. Both predictions occurred: the disruptive social effect in burnt habitat and the adaptive social response in adjacent unburnt habitat. The latter followed a massive demographic influx to unburnt 'refuge' habitat that increased competition for dens, leading to a density-related kin selection response. Our results show remarkable short-term plasticity of animal social behaviour and demonstrate how the social effects of disturbance extend into undisturbed habitat owing to landscape-scale demographic shifts. We predicted long-term changes in kinship-based cooperative behaviour resulting from the genetic and resource impacts of forecast changes to fire regimes in these forests.     

Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites

Complex eusocial insect societies are generally matrifilial, suggesting kin selection has been of importance in their development. For simpler social systems, factors favouring their existence, in particular kin selection, have rarely been studied. Communal nesting is one of these simple social organizations, and is found in a diversity of insect species. To examine whether kin selection may play a role in the evolution and maintenance of communality, we estimated genetic relatedness of nestmate females of the facultatively communal bee, Andrena jacobi . Microsatellite loci were developed for this species and used to analyse individuals from two populations. Loci were variable, they were in heterozygote deficit and showed positive inbreeding coefficients. This may arise from nonrandom mating; previous observations (Paxton & Tengö 1996) indicate that a large proportion of females mate intranidally with nestmate males in their natal nests before first emerging. Nestmate relatedness was low, no different from zero for all loci in one population and for three of four loci in the other population. The large number of nestmates sharing a common nest (up to 594) may explain the low relatedness estimates, although relatedness was also independent of the number of females sharing a nest. Lack of inclusive fitness payoffs could constrain social evolution in this communal species.     

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.