Catherine Crockford

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.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.

Female chacma baboons form strong, equitable, and enduring social bonds

Analyses of the pattern of associations, social interactions, coalitions, and aggression among chacma baboons (Papio hamadryas ursinus) in the Okavango Delta of Botswana over a 16-year period indicate that adult females form close, equitable, supportive, and enduring social relationships. They show strong and stable preferences for close kin, particularly their own mothers and daughters. Females also form strong attachments to unrelated females who are close to their own age and who are likely to be paternal half-sisters. Although absolute rates of aggression among kin are as high as rates of aggression among nonkin, females are more tolerant of close relatives than they are of others with whom they have comparable amounts of contact. These findings complement previous work which indicates that the strength of social bonds enhances the fitness of females in this population and support findings about the structure and function of social bonds in other primate groups.

Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.

Call combinations in wild chimpanzees

Summary By combining different call types, such as barks with screams, individuals have the potential to vastly increase the range of information that can be decoded by listeners. Few animal studies, however, have examined the information content of call combinations compared with the information conveyed by each call singularly. We examined several aspects of call combinations in the repertoire of wild chimpanzees in the Tai Forest, Ivory Coast, including the types of combinations, the contexts and possible functions and compared these with the use of single calls. Almost half of all vocalisations produced by the Tai chimpanzees occurred in combination with other vocalisations or with drumming. A total of 88 different types of combinations were used. Single calls and call combinations were each produced in specific contexts. The contexts in which six of ten combinations were produced differed from the contexts of at least one of the component calls. The contexts in which the combinations were produced varied from the component calls in five different ways, three having potentially novel functions. Two of the three may have an additive function, such that two pieces of information can be conveyed simultaneously, increasing message complexity. This analysis clearly shows that call combinations are an important part of chimpanzee communication. The implications with regard to the evolution of human language are discussed. Testing of the information conveyed by single calls and of call combinations, using playback experiments, is advocated.

Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review.

The neuropeptide, oxytocin, receives increasing attention due to its role in stress regulation and promoting affiliative social behavior. Research across mammals points to a complex pattern whereby social context and individual differences moderate the central release of oxytocin as well as moderate the effects that exogenous administration of oxytocin has on social behavior. In addition, it is becoming evident that measuring endogenous peripheral oxytocin levels is an informative tool. This is particularly so when oxytocin can be measured from non-invasively collected samples, such as in urine. Although it is still debated as to whether peripheral measures of oxytocin relate to central measures of oxytocin, anatomical and functional evidence indicate a link between the two. We argue that non-invasive measures of peripheral oxytocin hold several research and potential therapeutic advantages. Principally, study subjects can be sampled repeatedly in different social contexts where social history between interaction partners can be taken into account. Several hormones can be measured simultaneously allowing examination of the influence of oxytocin interactions with other hormones on motivational states. Valence of relationships as well as changes in relationship quality over time can be measured through endocrine responses. Also, the approach of identifying natural social contexts that are associated with endogenous oxytocin release offers the potential of behavioral therapy as an addition or alternative to chemical therapy in the field of mental health.

Vocal alliances in Chacma baboons (Papio hamadryas ursinus)

Theory predicts that females in species with matrilineal dominance hierarchies should use nepotistic support systems to maintain their family’s rank. Female Old World monkeys, however, form alliances against other females at surprisingly low rates. Nonetheless, in many species, females utter threat vocalizations when observing others’ disputes, suggesting that these vocalizations may function as ‘vocal alliances’. We describe a playback experiment testing the efficacy of vocal alliances in free-ranging female baboons. Subjects were played the same female’s threat-grunts under three separate conditions: after being threatened by the signaller’s close relative to mimic kin support, after being threatened by a female maternally unrelated to the signaller to mimic non-kin support, and after a friendly interaction with the signaller’s close relative as a control. Subjects responded more strongly to the playback and avoided the signaller and her matrilineal relatives for a longer period of time in kin support trials than in either non-kin support or no aggression trials. In contrast, there was no difference in subjects’ behaviour between non-kin support and no aggression trials. These results corroborate observational data showing that vocal support occurs at a higher rate than physical support in female baboons, and that kin are more likely to provide vocal support than non-kin. We conclude that vocal support plays a similar role as physical support in the alliances of female baboons.

Hedging their bets? Male and female chacma baboons form friendships based on likelihood of paternity

In chacma baboons (Papio hamadryas ursinus), adult males and lactating females form preferential associations, or ‘friendships’, that provide protection against potentially infanticidal attacks. Little is known about the mechanisms by which males and females form friendships, or the function of friendships for males. We examined the relationship between mating activity, paternity and friendships over a 3-year period. A male’s proportion of consort activity with a female within and outside of her period of most likely conception, along with his dominance rank, each contributed importantly in models of paternity outcomes and formation of friendships. In 87% of births, the male that monopolized the greatest proportion of a female’s consort days during her last conceptive cycle was the father of her offspring. In 82% of the births where the female’s primary consort partner was present at parturition, he became her friend. When the primary consort partner was absent at parturition, females formed friendships with males that had monopolized the second or third greatest proportion of their previous consort days. Similarly, 78% of males became friends with females with whom they had obtained their greatest consort success. Such a flexible strategy based on probabilistic assessment of paternity may be adaptive for females, given unpredictable fluctuations in male presence within the group. In a mating system with high dominance-based reproductive skew, males may benefit by investing preferentially in those infants that they are most likely to have fathered.

Assessing functional communication in aphasia: clinical utility and time demands of three methods

A variety of methods has recently been used to assess everyday communication abilities in aphasic adults. This study compares three such methods for their clinical utility and the amount of a therapists time they use. The three methods employed a standard rating schedule completed by relatives, analysis of speech elicited through role-play and a partial analysis of everyday conversation samples. The utility of these assessments as a clinical tool was measured in terms of the therapists time needed, and the assessments ability to show stability or change of communicative effectiveness on test-re-test measures and to illuminate areas for therapeutic intervention. Eight aphasic adults (five acute and three chronic) were tested on all three assessments, then re-tested after a period of 3 months. The results suggested that, although more time-consuming, the partial conversational analysis was a more sensitive measure of stability or change of communicative effectiveness over time than the other two measures, and had the potential advantage for indirect intervention of revealing conversational strategies used by the partner as well as those used by the aphasic individual.