Joan B. Silk

Chimpanzees are indifferent to the welfare of unrelated group members.

Humans are an unusually prosocial species—we vote, give blood, recycle, give tithes and punish violators of social norms. Experimental evidence indicates that people willingly incur costs to help strangers in anonymous one-shot interactions, and that altruistic behaviour is motivated, at least in part, by empathy and concern for the welfare of others (hereafter referred to as other-regarding preferences). In contrast, cooperative behaviour in non-human primates is mainly limited to kin and reciprocating partners, and is virtually never extended to unfamiliar individuals. Here we present experimental tests of the existence of other-regarding preferences in non-human primates, and show that chimpanzees (Pan troglodytes) do not take advantage of opportunities to deliver benefits to familiar individuals at no material cost to themselves, suggesting that chimpanzee behaviour is not motivated by other-regarding preferences. Chimpanzees are among the primates most likely to demonstrate prosocial behaviours. They participate in a variety of collective activities, including territorial patrols, coalitionary aggression, cooperative hunting, food sharing and joint mate guarding. Consolation of victims of aggression and anecdotal accounts of solicitous treatment of injured individuals suggest that chimpanzees may feel empathy. Chimpanzees sometimes reject exchanges in which they receive less valuable rewards than others, which may be one element of a ‘sense of fairness’, but there is no evidence that they are averse to interactions in which they benefit more than others.

The adaptive value of sociality in mammalian groups

According to behavioural ecology theory, sociality evolves when the net benefits of close association with conspecifics exceed the costs. The nature and relative magnitude of the benefits and costs of sociality are expected to vary across species and habitats. When sociality is favoured, animals may form groups that range from small pair-bonded units to huge aggregations. The size and composition of social groups have diverse effects on morphology and behaviour, ranging from the extent of sexual dimorphism to brain size, and the structure of social relationships. This general argument implies that sociality has fitness consequences for individuals. However, for most mammalian species, especially long-lived animals like primates, there are sizable gaps in the chain of evidence that links sociality and social bonds to fitness outcomes. These gaps reflect the difficulty of quantifying the cumulative effects of behavioural interactions on fitness and the lack of information about the nature of social relationships among individuals in most taxa. Here, I review what is known about the reproductive consequences of sociality for mammals.

The benefits of social capital: close social bonds among female baboons enhance offspring survival

Sociality has evolved in many animal taxa, but primates are unusual because they establish highly differentiated bonds with other group members. Such bonds are particularly pronounced among females in species like baboons, with female philopatry and male dispersal. These relationships seem to confer a number of short-term benefits on females, and sociality enhances infant survival in some populations. However, the long-term consequences of social bonds among adult females have not been well established. Here we provide the first direct evidence that social relationships among female baboons convey fitness benefits. In a group of free-ranging baboons, Papio cynocephalus ursinus, the offspring of females who formed strong social bonds with other females lived significantly longer than the offspring of females who formed weaker social bonds. These survival benefits were independent of maternal dominance rank and number of kin and extended into offspring adulthood. In particular, females who formed stronger bonds with their mothers and adult daughters experienced higher offspring survival rates than females who formed weaker bonds. For females lacking mothers or adult daughters, offspring survival was closely linked to bonds between maternal sisters. These results parallel those from human studies, which show that greater social integration is generally associated with reduced mortality and better physical and mental health, particularly for women.

Social relationships among adult female baboons (papio cynocephalus) I. Variation in the strength of social bonds

Sociality has positive effects on female fitness in many mammalian species. Among female baboons, those who are most socially integrated reproduce most successfully. Here we test a number of predictions derived from kin selection theory about the strength of social bonds among adult female baboons. Our analyses are based on systematic observations of grooming and association patterns among 118 females living in seven different social groups in the Amboseli Basin of Kenya over a 16-year period. Females in these groups formed the strongest bonds with close kin, including their mothers, daughters, and maternal and paternal sisters. Females were also strongly attracted toward females who were close to their own age, perhaps because peers were often paternal sisters. Females’ bonds with their maternal sisters were strengthened after their mother’s deaths, whereas their relationships with their maternal aunts were weakened after their mother’s death. In addition, females formed stronger bonds with their paternal sisters when no close maternal kin were available, and they compensated for the absence of any close kin by forming strong bonds with nonrelatives. Taken together, these data suggest that social bonds play a vital role in females’ lives, and the ability to establish and maintain strong social bonds may have important fitness consequences for females.

True paternal care in a multi-male primate society

Although male parental care is rare among mammals, adult males of many cercopithecine primate species provide care for infants and juveniles. This care is often in the form of grooming, carrying, support in agonistic interactions, and protection against infanticide. For these behaviours to be interpreted as true parental care, males must selectively direct care towards their own offspring and this care must result in fitness benefits. With the exception of males defending probable offspring from infanticide, male primates living in multi-male, multi-female social groups have not been shown to selectively direct care towards their own offspring. We determined paternity for 75 juveniles in a population of wild savannah baboons (Papio cynocephalus) and collected data on interventions in agonistic disputes by adult males on behalf of juveniles as a form of male care. Here we show that adult males differentiate their offspring from unrelated juveniles and selectively support their offspring in agonistic disputes. As support in agonistic disputes is likely to contribute to rank acquisition and protect juveniles from injury and stress, this can be considered true parental care.

Local Resource Competition and Facultative Adjustment of Sex Ratios in Relation to Competitive Abilities

I have suggested that local resource competition and male dispersal may generally lead to (1) intense competition among females for resources and reproductive opportunities, (2) limiting the recruitment of females, (3) extensive maternal investment in vulnerable female offspring, and (4) facultative adjustment of the sex ratio of progeny in relation to maternal competitive abilities. This argument appears to be consistent with evidence drawn from several species of macaques and baboons. The size of groups appears to be limited by the availability of resources; females actively compete over access to resources, and limit the number of females born and raised in their groups through the effective harassment of females carrying female fetuses and immature females. In response to such harassment, females appear to invest more in their daughters than sons, and to adjust the sex ratio of their progeny in relation to the expected reproductive success of their sons and daughters. High ranking females whose female progeny are likely to survive to become high ranking, reproductively successful adults produce more daughters than sons; while low ranking females whose female offspring are unlikely to survive to maturity or to reproduce successfully, produce more sons than daughters.

Social Components of Fitness in Primate Groups

There is much interest in the evolutionary forces that favored the evolution of large brains in the primate order. The social brain hypothesis posits that selection has favored larger brains and more complex cognitive capacities as a means to cope with the challenges of social life. The hypothesis is supported by evidence that shows that group size is linked to various measures of brain size. But it has not been clear how cognitive complexity confers fitness advantages on individuals. Research in the field and laboratory shows that sophisticated social cognition underlies social behavior in primate groups. Moreover, a growing body of evidence suggests that the quality of social relationships has measurable fitness consequences for individuals.

Altruism among female Macaca radiata: explanations and analysis of patterns of grooming and coalition formation.

Analysis of the observed patterns of two forms of putative altruism (grooming and coalition formation) among adult female members of a group of captive bonnet macaques (Macaca radiata) indicates that both kinship and dominance rank influence the distribution and rate of these behaviors. Females groom their adult relatives more often and more reciprocally than they groom unrelated females of similar ranks. In addition, females are more likely to support their relatives than nonrelatives and are likely to incur greater risks when they do so. Grooming and coalition formation do not occur exclusively among kin. Females primarily groom higher ranking females and support unrelated females against females lower ranking than themselves. Although females do not preferentially support unrelated females that groom or support them most, they do refrain from harassing lower ranking females that are currently grooming them or a female higher ranking than themselves. Thus, by grooming a higher ranking female a female reduces the probability that she will be harassed by other females. The relationship of these results to predictions derived from several different sociobiological hypotheses is discussed.

Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds

A growing body of evidence suggests that social bonds have adaptive value for animals that live in social groups. Although these findings suggest that natural selection may favor the ability to cultivate and sustain social bonds, we know very little about the factors that influence the quality or stability of social bonds. Here, we draw on data derived from a 16-year study of baboons living in seven different social groups in the Amboseli basin of Kenya to evaluate the quality and stability of social bonds among females. Our results extend previous analyses, which demonstrate that females form the strongest bonds with close maternal and paternal kin, age mates (who may be paternal kin), and females who occupy similar ranks but are not maternal relatives. Here we show that the same factors influence the quality and strength of social bonds. Moreover, the results demonstrate that the quality of social bonds directly affects their stability.

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. Hamiltons 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.