Estimates of relatedness in groups of humpback whales (Megaptera novaeangliae) on two wintering grounds of the Southern Hemisphere

Group formation in humpback whales has been described in relation to different components of the migratory cycle, yet it is debated whether such groups represent real social bonding or ephemeral aggregations. Cooperative behaviours are exhibited during feeding activities, and it has been suggested that males may cooperate during competition for mates. Since most cooperative behaviours are expected to originate among kin, genetic relatedness represents a critical variable in the understanding of any social phenomenon, especially when cooperation cannot be confirmed unequivocally. Using an approach combining multi-locus microsatellite genotyping and several genetic relatedness estimators, we analyzed whale associations for two different wintering grounds in the Southern Hemisphere. The analyses included 648 whales sampled from 292 groups off the coast of Gabon and Northeast Madagascar, and screened for eleven microsatellite loci. Through simulations, we assessed the performance of three pairwise relatedness estimators. The individuals were molecularly sexed and their associations were investigated in the context of sex and group type. No significant association among relatives was found with the exception of mother-offspring pairs, supporting previous indications of extended maternal care. The analysis from the Gabon population also suggests that related males may avoid each other during competitive activities. Our results demonstrate that if cooperative behaviours occur on wintering grounds they are not favoured by kin selection.     

Reciprocal altruism in bats and other mammals

In this paper five conditions are specified which must be met before reciprocal altruism, rather than kin selection, should be invoked. Four purported mammalian examples— social grooming in coati, cluster position in roosting pallid bats, information exchange among greater spear-nosed bats, and blood regurgitation among vampire bats—are examined to determine if reciprocal altruism is necessary to plausibly explain each situation. Results from a computer simulation which apportions the relative selective advantage of vampire bat food sharing to kin selection and reciprocal altruism are then presented. The results demonstrate that the increase in individual survivorship due to reciprocal food sharing events in this species provides a greater increase in inclusive fitness than can be attributed to aiding relatives. This analysis suggests that reciprocal altruism can be selectively more important than kin selection when altruistic behaviors in a relatively large social group occur frequently and provide a major fitness benefit to the recipient even when that recipient is related to the donor.     

Non-song acoustic communication in migrating humpback whales (Megaptera novaeangliae)

Humpback whales are renowned for the complex structured songs produced by males. A second, relatively understudied area of humpback acoustic communication concerns un-patterned sounds known as "social sounds," produced by both males and females. These include vocalizations as well as sounds produced at the surface of the water as a result of surface behaviors ( e.g. , breaching, pectoral slapping). This study describes a portion of the non-song social sound repertoire of southward migrating humpbacks in Australian waters, and explores the social relevance of these sounds. On migration, humpback whales travel in social groups of varying compositions. These social groups are not stable in that humpback whales continually change group composition by splitting from, or joining with, other groups. The results of this study suggest that "breaching" and "slapping" have a communicative function. Other sounds such as "underwater blows" and "cries" were heard mainly in competitive groups while other low-frequency sounds such as "grumbles,""snorts,""thwops," and "wops" may function in intra- or inter-group communication. Particular sounds ("grunts,""groans," and "barks") were almost exclusive to joining pods suggesting a role in social integration. Social sounds in humpbacks may have specific social and behavioral functions relating to social group composition, and the mediation of interactions between these social groups.     

Kin recognition and the evolution of altruism

In 1964, Hamilton formalized the idea of kin selection to explain the evolution of altruistic behaviours. Since then, numerous examples from a diverse array of taxa have shown that seemingly altruistic actions towards close relatives are a common phenomenon. Although many species use kin recognition to direct altruistic behaviours preferentially towards relatives, this important aspect of social biology is less well understood theoretically. I extend Hamilton's classic work by defining the conditions for the evolution of kin-directed altruism when recognizers are permitted to make acceptance (type I) and rejection (type II) errors in the identification of social partners with respect to kinship. The effect of errors in recognition on the evolution of kin-directed altruism depends on whether the population initially consists of unconditional altruists or non-altruists (i.e. alternative forms of non-recognizers). Factors affecting the level of these error rates themselves, their evolution and their long-term stability are discussed.     

Kinship of long-term associates in the highly social sperm whale

The evolution of stable social groups can be promoted by both indirect and direct fitness benefits. Sperm whales (Physeter macrocephalus) are highly social, with a hierarchical social structure based around core groups of adult females and subadults, a rare level of complexity among mammals. We combined long-term satellite tracking (ranging from 11 to 607 days) of 51 individual sperm whales with genetic kinship analysis to assess the pattern of kin associations within and among coherent social units. Unlike findings for other species with similar social structure, we find no consistent correlation between kinship and association apart from close associations between two pairs of first-order relatives. A third pair of first-order relatives did not associate, and overall, the mean relatedness was the same within as among social groups. However, social behaviour can also be promoted by ecological factors such as resource dispersion. We assessed putative foraging behaviour during travel from the satellite-tracking data, which suggested that prey resources were dispersed and unpredictable, a condition that could promote living in groups.     

Hamilton's rule and kin competition: the Kipsigis case

Evolutionary studies of human behavior have emphasized the importance of kin selection in explaining social institutions and fitness outcomes. Our relatives can nevertheless be competitors as well as sources of altruism. This is particularly likely when there is local competition over resources, where conflict can lead to strife among nondispersing relatives, reducing or even negating the effects of relatedness on promoting altruism. Here, I present demographic data on a land-limited human population, utilizing large within-population variation in land ownership to determine the interactions between local resource competition and the benefits of kin in enhancing child survival, a key component of fitness in this population. As predicted, wealth affects the extent of kin altruism, in that paternal relatives (specifically father's brothers) appear to buffer young children from mortality much more effectively in rich than in poor households. This interaction effect is interpreted as evidence that the extent of nepotism among humans depends critically on resource availability. Further unanticipated evidence that maternal kin play a role in buffering children from mortality in situations where paternal kin control few resources speaks to the important role that specific local circumstance plays in shaping kin contributions to child welfare.     

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.     

Demography, altruism, and the benefits of budding

It is now widely appreciated that competition between kin inhibits the evolution of altruism. In standard population genetics models, it is difficult for indiscriminate altruism towards social partners to be favoured at all. The reason is that while limited dispersal increases the kinship of social partners it also intensifies local competition. One solution that has received very little attention is if individuals disperse as groups (budding dispersal), as this relaxes local competition without reducing kinship. Budding behaviour is widespread through all levels of biological organization, from early protocellular life to cooperatively breeding vertebrates. We model the effects of individual dispersal, budding dispersal, soft selection and hard selection to examine the conditions under which altruism is favoured. More generally, we examine how these various demographic details feed into relatedness and scale of competition parameters that can be included into Hamilton's rule.     

Evidence for the functions of surface‐active behaviors in humpback whales (Megaptera novaeangliae)

As part of their social sound repertoire, migrating humpback whales (Megaptera novaeangliae) perform a large variety of surface‐active behaviors, such as breaching and repetitive slapping of the pectoral fins and tail flukes; however, little is known about what factors influence these behaviors and what their functions might be. We investigated the potential functions of surface‐active behaviors in humpback whale groups by examining the social and environmental contexts in which they occurred. Focal observations on 94 different groups of whales were collected in conjunction with continuous acoustic monitoring, and data on the social and environmental context of each group. We propose that breaching may play a role in communication between distant groups as the probability of observing this behavior decreased significantly when the nearest whale group was within 4,000 m compared to beyond 4,000 m. Involvement in group interactions, such as the splitting of a group or a group joining with other whales, was an important factor in predicting the occurrence of pectoral, fluke, and peduncle slapping, and we suggest that they play a role in close‐range or within‐group communication. This study highlights the potentially important and diverse roles of surface‐active behaviors in the communication of migrating humpback whales.     

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.     

Population viscosity can promote the evolution of altruistic sterile helpers and eusociality

Because it increases relatedness between interacting individuals, population viscosity has been proposed to favour the evolution of altruistic helping. However, because it increases local competition between relatives, population viscosity may also act as a brake for the evolution of helping behaviours. In simple models, the kin selected fecundity benefits of helping are exactly cancelled out by the cost of increased competition between relatives when helping occurs after dispersal. This result has lead to the widespread view, especially among people working with social organisms, that special conditions are required for the evolution of altruism. Here, we re-examine this result by constructing a simple population genetic model where we analyse whether the evolution of a sterile worker caste (i.e. an extreme case of altruism) can be selected for by limited dispersal. We show that a sterile worker caste can be selected for even under the simplest life-cycle assumptions. This has relevant consequences for our understanding of the evolution of altruism in social organisms, as many social insects are characterized by limited dispersal and significant genetic population structure.     

Kin encounter rate and inbreeding avoidance in canids

Mating with close kin can lead to inbreeding depression through the expression of recessive deleterious alleles and loss of heterozygosity. Mate selection may be affected by kin encounter rate, and inbreeding avoidance may not be uniform but associated with age and social system. Specifically, selection for kin recognition and inbreeding avoidance may be more developed in species that live in family groups or breed cooperatively. To test this hypothesis, we compared kin encounter rate and the proportion of related breeding pairs in noninbred and highly inbred canid populations. The chance of randomly encountering a full sib ranged between 1-8% and 20-22% in noninbred and inbred canid populations, respectively. We show that regardless of encounter rate, outside natal groups mates were selected independent of relatedness. Within natal groups, there was a significant avoidance of mating with a relative. Lack of discrimination against mating with close relatives outside packs suggests that the rate of inbreeding in canids is related to the proximity of close relatives, which could explain the high degree of inbreeding depression observed in some populations. The idea that kin encounter rate and social organization can explain the lack of inbreeding avoidance in some species is intriguing and may have implications for the management of populations at risk.     

Altruism via kin-selection strategies that rely on arbitrary tags with which they coevolve

Hamilton's rule explains when natural selection will favor altruism between conspecifics, given their degree of relatedness. In practice, indicators of relatedness (such as scent) coevolve with strategies based on these indicators, a fact not included in previous theories of kin recognition. Using a combination of simulation modeling and mathematical extension of Hamilton's rule, we demonstrate how altruism can emerge and be sustained in a coevolutionary setting where relatedness depends on an individual's social environment and varies from one locus to another. The results support a very general expectation of widespread, and not necessarily weak, conditional altruism in nature.     

Cultural relatedness under oblique and horizontal transmission rules

The concept of genetic relatedness is central to the sociobiological theory of kinship altruism. Genes which code for altruistic acts toward closely related genetic kin can overcome selection pressures favoring self-interested behavior. But genetic relatedness declines rapidly as kinship becomes more distant, thereby restricting genetically-based altruism to very close kin. This paper extends these notions to cultural relatedness, arguing that oblique and horizontal transmission can yield high levels of cultural relatedness in larger groups. A mathematical model of cultural transmission is proposed, and equilibria for several special cases are investigated. For all models, the equilibrium level of relatedness is critically dependent on the influence of exogenous sources. In models with equal influence of nonparents, the level of relatedness varies inversely with group size. On the other hand, when nonparental influence is concentrated on a single individual, the level of relatedness does not vary with group size.     

The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants

Many social animals live in stable groups. In contrast, African savannah elephants (Loxodonta africana) live in unusually fluid, fission-fusion societies. That is, 'core' social groups are composed of predictable sets of individuals; however, over the course of hours or days, these groups may temporarily divide and reunite, or they may fuse with other social groups to form much larger social units. Here, we test the hypothesis that genetic relatedness predicts patterns of group fission and fusion among wild, female African elephants. Our study of a single Kenyan population spans 236 individuals in 45 core social groups, genotyped at 11 microsatellite and one mitochondrial DNA (mtDNA) locus. We found that genetic relatedness predicted group fission; adult females remained with their first order maternal relatives when core groups fissioned temporarily. Relatedness also predicted temporary fusion between social groups; core groups were more likely to fuse with each other when the oldest females in each group were genetic relatives. Groups that shared mtDNA haplotypes were also significantly more likely to fuse than groups that did not share mtDNA. Our results suggest that associations between core social groups persist for decades after the original maternal kin have died. We discuss these results in the context of kin selection and its possible role in the evolution of elephant sociality.     

Kin-biased distribution in brown trout: an effect of redd location or kin recognition?

A wide range of animals have been reported to show kin-biased behaviours, such as reduced aggressiveness and increased food sharing among relatives. However, less is known about whether wild animals also associate with relatives under natural conditions, which is a prerequisite to facilitate kin-biased behaviours and hence kin selection. We tested, by means of microsatellite polymorphism, correlations between pair-wise relatedness and pair-wise metric distance in wild brown trout (Salmo trutta L.) under natural conditions in two streams. Our data show that young-of-the-year as well as older trout found close together also had a higher genetic relatedness in one of the two streams, whereas no relationship was found in the other stream. Very few half and full siblings were found in the second stream and under these conditions it is unlikely that kin-biased behaviours will receive positive selection. We discuss the underlying mechanisms for the observed structure and we specifically address the issue of whether the grouping of related individuals could reflect dispersal from the same spawning redds, or if it reflects active association with relatives, possibly conferring kin-selected advantages.     

Kin selection is the key to altruism

Kin selection theory, also known as inclusive fitness theory, has been the subject of much debate and misunderstanding. Nevertheless, the idea that relatedness among individuals can drive the evolution of altruism has emerged as a central paradigm in evolutionary biology. Or has it? In two recent articles, E.O. Wilson argues that kin selection should no longer be considered the main explanation for the evolution of altruism in insect societies. Here, we discuss what these articles say about kin selection and how it relates to the theory. We conclude that kin selection remains the key explanation for the evolution of altruism in eusocial insects.     

The evolution of trans-generational altruism: kin selection meets niche construction

A cornerstone result of sociobiology states that limited dispersal can induce kin competition to offset the kin selected benefits of altruism. Several mechanisms have been proposed to circumvent this dilemma but all assume that actors and recipients of altruism interact during the same time period. Here, this assumption is relaxed and a model is developed where individuals express an altruistic act, which results in posthumously helping relatives living in the future. The analysis of this model suggests that kin selected benefits can then feedback on the evolution of the trait in a way that promotes altruistic helping at high rates under limited dispersal. The decoupling of kin competition and kin selected benefits results from the fact that by helping relatives living in the future, an actor is helping individuals that are not in direct competition with itself. A direct consequence is that behaviours which actors gain by reducing the common good of present and future generations can be opposed by kin selection. The present model integrates niche-constructing traits with kin selection theory and delineates demographic and ecological conditions under which altruism can be selected for; and conditions where the 'tragedy of the commons' can be reduced.     

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.     

Genetic relatedness in wintering groups of house sparrows (Passer domesticus)

Social behaviour of group-living animals is often influenced by the relatedness of individuals, thus understanding the genetic structure of groups is important for the interpretation of costs and benefits of social interactions. In this study, we investigated genetic relatedness in feeding aggregations of free-living house sparrows ( Passer domesticus ) during the nonbreeding season. This species is a frequent model system for studies of social behaviour (e.g. aggression, social foraging), but we lack adequate information on the kin structure of sparrow flocks. During two winters, we ringed and observed sparrows at feeding stations, and used resightings to identify stable flock-members and to calculate association indices between birds. We genotyped the birds using seven highly polymorphic microsatellite loci, and estimated pairwise relatedness coefficients and relatedness categories (close kin vs. unrelated) by maximum likelihood method. We found that most birds were unrelated to each other in the flocks (mean ± SE relatedness coefficient: 0.06 ± 0.002), although most individuals had at least a few close relatives in their home flock (14.3 ± 0.6% of flock-mates). Pairwise association between individuals was not significantly related to their genetic relatedness. Furthermore, there was no difference between within-flock vs. between-flock relatedness, and birds had similar proportions of close kin within and outside their home flock. Finally, relatedness among members of different flocks was unrelated to the distance between their flocks. Thus, sparrow flocks were not characterized by association of relatives, nevertheless the presence of some close kin may provide opportunity for kin-biased behaviours to evolve.