Animal behavior: A tale of two apes.

A new paper shows that rates of aggression are higher, and rates of coalition formation are lower, among male bonobos than among male chimpanzees. These findings are noteworthy because they challenge the view that female bonobos' preferences for less aggressive males favored a reduction in male aggression and an increase in social tolerance.

Between-group cooperation in bonobos.

Bonobos provide insight into the origins of partner-specific cooperation in human groups.

Tradeoffs between mating effort and parenting effort in a polygynandrous mammal.

Reproductive strategies are defined by expenditures of time and energy devoted to mating effort, which increases mating opportunities, and parenting effort, which enhances the survival of offspring. We examine tradeoffs between mating effort and parenting effort in male olive baboons, Papio anubis, a species in which males compete for mating opportunities, but also form ties to lactating females (primary associations) that represent a form of parenting effort. Males that are involved in more primary associations invest less in mating effort than males who are involved in fewer primary associations. Males that are involved in more primary associations play a smaller role in establishing proximity to their primary associates than other males, suggesting that males operate under temporal constraints. There is also some evidence that involvement in primary associations negatively affects paternity success. Taken together, the data suggest that males face tradeoffs between mating effort and parenting effort.

Sex differences in cooperative coalitions: a mammalian perspective.

In group-living species, cooperative tactics can offset asymmetries in resource-holding potential between individuals and alter the outcome of intragroup conflicts. Differences in the kinds of competitive pressures that males and females face might influence the benefits they gain from forming intragroup coalitions. We predicted that there would be a female bias in intragroup coalitions because females (1) are more like to live with kin than males are, and (2) compete over resources that are more readily shared than resources males compete over. We tested this main prediction using information about coalition formation across mammalian species and phylogenetic comparative analyses. We found that for nearly all species in which intragroup coalitions occur, members of both sexes participate, making this the typical mammalian pattern. The presence and frequency of female or male coalitions were not strongly associated with key socio-ecological factors like resource defensibility, sexual dimorphism or philopatry. This suggests that once the ability to form intragroup coalitions emerges in one sex, it is likely to emerge in the other sex as well and that there is no strong phylogenetic legacy of sex differences in this form of cooperation. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

No strong evidence for universal gender differences in the development of cooperative behaviour across societies.

Human cooperation varies both across and within societies, and developmental studies can inform our understanding of the sources of both kinds of variation. One key candidate for explaining within-society variation in cooperative behaviour is gender, but we know little about whether gender differences in cooperation take root early in ontogeny or emerge similarly across diverse societies. Here, we explore two existing cross-cultural datasets of 4- to 15-year-old children's preferences for equality in experimental tasks measuring prosociality (14 societies) and fairness (seven societies), and we look for evidence of (i) widespread gender differences in the development of cooperation, and (ii) substantial societal variation in gender differences. This cross-cultural approach is crucial for revealing universal human gender differences in the development of cooperation, and it helps answer recent calls for greater cultural diversity in the study of human development. We find that gender has little impact on the development of prosociality and fairness within these datasets, and we do not find much evidence for substantial societal variation in gender differences. We discuss the implications of these findings for our knowledge about the nature and origin of gender differences in cooperation, and for future research attempting to study human development using diverse cultural samples. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Pathways to paternal care in primates.

Natural selection will favor male care when males have limited alternative mating opportunities, can invest in their own offspring, and when care enhances males' fitness. These conditions are easiest to fulfill in pair-bonded species, but neither male care nor stable "breeding bonds" that facilitate it are limited to pair-bonded species. We review evidence of paternal care and extended breeding bonds in owl monkeys, baboons, Assamese macaques, mountain gorillas, and chimpanzees. The data, which span social/mating systems and ecologies, suggest that there are multiple pathways by which conditions conducive to male care can arise. This diversity highlights the difficulty of making inferences about the emergence of male care in early hominins based on single traits visible in the fossil record. We discuss what types of data are most needed and the questions yet to be answered about the evolution of male care and extended breeding bonds in the primate order.

Early life adversity has long-term effects on sociality and interaction style in female baboons.

Social bonds enhance fitness in many group-living animals, generating interest in the processes that create individual variation in sociality. Previous work on female baboons shows that early life adversity and temperament both influence social connectedness in adulthood. Early life adversity might shape sociality by reducing ability to invest in social relationships or through effects on attractiveness as a social partner. We examine how females' early life adversity predicts sociality and temperament in wild olive baboons, and evaluate whether temperament mediates the relationship between early life adversity and sociality. We use behavioural data on 31 females to quantify sociality. We measure interaction style as the tendency to produce grunts (signals of benign intent) in contexts in which the vocalization does not produce immediate benefits to the actor. Early life adversity was negatively correlated with overall sociality, but was a stronger predictor of social behaviours received than behaviours initiated. Females who experienced less early life adversity had more benign interaction styles and benign interaction styles were associated with receiving more social behaviours. Interaction style may partially mediate the association between early life adversity and sociality. These analyses add to our growing understanding of the processes connecting early life experiences to adult sociality.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Social norms and cultural diversity in the development of third-party punishment.

Human cooperation is probably supported by our tendency to punish selfishness in others. Social norms play an important role in motivating third-party punishment (TPP), and also in explaining societal differences in prosocial behaviour. However, there has been little work directly linking social norms to the development of TPP across societies. In this study, we explored the impact of normative information on the development of TPP in 603 children aged 4-14, across six diverse societies. Children began to perform TPP during middle childhood, and the developmental trajectories of this behaviour were similar across societies. We also found that social norms began to influence the likelihood of performing TPP during middle childhood in some of these societies. Norms specifying the punishment of selfishness were generally more influential than norms specifying the punishment of prosocial behaviour. These findings support the view that TPP of selfishness is important in all societies, and its development is shaped by a shared psychology for responding to normative information. Yet, the results also highlight the important role that children's prior knowledge of local norms may play in explaining societal variation in the development of both TPP and prosociality.

Shifts in Male Reproductive Tactics over the Life Course in a Polygynandrous Mammal.

In polygynous and polygynandrous species, there is often intense male-male competition over access to females, high male reproductive skew, and more male investment in mating effort than parenting effort [1]. However, the benefits derived from mating effort and parenting effort may change over the course of males' lives. In many mammalian species, there is a ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older males [2-8] and sire more infants [9-12]. Thus, males might derive more benefits from parenting effort than mating effort as they age and their competitive abilities decline [13]. Alternatively, older males may invest more effort in making themselves attractive to females as mates [14]. One way that older males might do so is by developing relationships with females and providing care for their offspring [14, 15]. Savannah baboons provide an excellent opportunity to test these hypotheses. They form stable multi-male, multi-female groups, and males compete for high ranking positions. In yellow and chacma baboons (Papio cynocephalus and P. ursinus), there is a ∩-shaped relationship between male age and dominance rank [12], and high rank enhances paternity success [12, 16]. Lactating female baboons form close ties ("primary associations" hereafter) with particular males [15-20], who support them and their infants in conflicts [15, 19] and buffer their infants from rough handling [20]. Females' primary associates are often, but not always, the sires of their current infants [16, 20-22].

Universal norm psychology leads to societal diversity in prosocial behaviour and development.

Recent studies have proposed that social norms play a key role in motivating human cooperation and in explaining the unique scale and cultural diversity of our prosociality. However, there have been few studies that directly link social norms to the form, development and variation in prosocial behaviour across societies. In a cross-cultural study of eight diverse societies, we provide evidence that (1) the prosocial behaviour of adults is predicted by what other members of their society judge to be the correct social norm, (2) the responsiveness of children to novel social norms develops similarly across societies and (3) societally variable prosocial behaviour develops concurrently with the responsiveness of children to norms in middle childhood. These data support the view that the development of prosocial behaviour is shaped by a psychology for responding to normative information, which itself develops universally across societies.

The evolution of human cooperation.

Darwin viewed cooperation as a perplexing challenge to his theory of natural selection. Natural selection generally favors the evolution of behaviors that enhance the fitness of individuals. Cooperative behavior, which increases the fitness of a recipient at the expense of the donor, contradicts this logic. William D. Hamilton helped to solve the puzzle when he showed that cooperation can evolve if cooperators direct benefits selectively to other cooperators (i.e. assortment). Kinship, group selection and the previous behavior of social partners all provide mechanisms for assortment (Figure 1), and kin selection and reciprocal altruism are the foundation of the kinds of cooperative behavior observed in many animals. Humans also bias cooperation in favor of kin and reciprocating partners, but the scope, scale, and variability of human cooperation greatly exceed that of other animals. Here, we introduce derived features of human cooperation in the context in which they originally evolved, and discuss the processes that may have shaped the evolution of our remarkable capacity for cooperation. We argue that culturally-evolved norms that specify how people should behave provide an evolutionarily novel mechanism for assortment, and play an important role in sustaining derived properties of cooperation in human groups.

Male-female relationships in olive baboons (Papio anubis): Parenting or mating effort?

Long-term male-female bonds and bi-parental investment in offspring are hallmarks of human society. A key question is how these traits evolved from the polygynandrously mating multimale multifemale society that likely characterized the Pan-Homo ancestor. In all three species of savanna baboons, lactating females form strong ties (sometimes called "friendships") with one or more adult males. For yellow baboons (Papio cynocephalus) and chacma baboons (Papio ursinus), several lines of evidence suggest that these relationships are a form of male parenting effort. In olive baboons (Papio anubis), females are thought to preferentially mate with their "friends", and male-female bonds may thus function as a form of mating effort. Here, we draw on behavioral and genetic data to evaluate the factors that shape male-female relationships in a well-studied population of olive baboons. We find support for the parenting effort hypothesis in that sires have stronger bonds with their infants' mothers than do other males. These bonds sometimes persist past weaning age and, in many cases, the sire of the previous infant is still a close partner of the female when she nurses her subsequent offspring. We find that males who have the strongest bonds with females that have resumed cycling, but are not currently sexually receptive, are more likely to sire the female's next offspring but the estimate is associated with large statistical uncertainty. We also find that in over one third of the cases, a female's successive infants were sired by the same male. Thus, in olive baboons, the development of stable breeding bonds and paternal investment seem to be grounded in the formation of close ties between males and anestrous females. However, other factors such as male dominance rank also influence paternity success and may preclude stability of these bonds to the extent found in human societies.

To grunt or not to grunt: Factors governing call production in female olive baboons, Papio anubis.

Vocal signals often play an important role in synchronizing the activities of group members, coordinating decisions about when and where to travel, and facilitating social interactions in which there are potential conflicts of interest. Here, we show that when female olive baboons (Papio anubis) give low amplitude grunts after approaching other females, they are less likely to behave aggressively toward their partners and more likely to handle their partners' infants and interact affiliatively with them. In addition, females are more likely to grunt after they approach lower ranking females than after they approach higher ranking females and are less likely to grunt after they approach their own mothers and daughters than after they approach other females. These patterns, which are strikingly similar to patterns previously reported in chacma baboons (Papio ursinus) support the hypothesis that grunts function as signals of benign intent. Moreover, they suggest that actors' decisions about whether to grunt or remain silent are influenced by the social context, particularly their partners' likely response to their approach. Taken together, the patterning of grunts in olive and chacma baboon suggests that these vocalizations play an important in reducing uncertainty about actors' intentions and facilitate nonaggressive social interactions.

Strategic Use of Affiliative Vocalizations by Wild Female Baboons.

Although vocal production in non-human primates is highly constrained, individuals appear to have some control over whether to call or remain silent. We investigated how contextual factors affect the production of grunts given by wild female chacma baboons, Papio ursinus, during social interactions. Females grunted as they approached other adult females 28% of the time. Supporting previous research, females were much more likely to grunt to mothers with young infants than to females without infants. Grunts also significantly increased the likelihood of affiliative interactions among all partners. Notably, however, grunts did not simply mirror existing social bonds. Instead, they appeared to perform a very different function: namely, to serve as signals of benign intent between partners whose relationship is not necessarily close or predictable. Females were less likely to grunt to their mothers or adult daughters-the individuals with whom they shared the closest and least aggressive bonds-than to other females. In contrast, patterns of grunting between sisters were similar to those between nonkin, perhaps reflecting sisters' more ambivalent relationships. Females grunted at higher rates to lower-ranking, than to higher-ranking, females, supporting the hypothesis that grunts do not simply signal the signaler's level of arousal or anxiety about receiving aggression, but instead function as signals of benign intent. Taken together, results suggest that the grunts given by female baboons serve to reduce uncertainty about the likely outcome of an interaction between partners whose relationship is not predictably affiliative. Despite their limited vocal repertoire, baboons appear to be skilled at modifying call production in different social contexts and for different audiences.

Network connections, dyadic bonds and fitness in wild female baboons.

In many social mammals, females who form close, differentiated bonds with others experience greater offspring survival and longevity. We still know little, however, about how females' relationships are structured within the social group, or whether connections beyond the level of the dyad have any adaptive value. Here, we apply social network analysis to wild baboons in order to evaluate the comparative benefits of dyadic bonds against several network measures. Results suggest that females with strong dyadic bonds also showed high eigenvector centrality, a measure of the extent to which an individual's partners are connected to others in the network. Eigenvector centrality was a better predictor of offspring survival than dyadic bond strength. Previous results have shown that female baboons derive significant fitness benefits from forming close, stable bonds with several other females. Results presented here suggest that these benefits may be further augmented if a female's social partners are themselves well connected to others within the group rather than being restricted to a smaller clique.

Infant Mortality Risk and Paternity Certainty Are Associated with Postnatal Maternal Behavior toward Adult Male Mountain Gorillas (Gorilla beringei beringei).

Sexually selected infanticide is an important source of infant mortality in many mammalian species. In species with long-term male-female associations, females may benefit from male protection against infanticidal outsiders. We tested whether mountain gorilla (Gorilla beringei beringei) mothers in single and multi-male groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center actively facilitated interactions between their infants and a potentially protective male. We also evaluated the criteria mothers in multi-male groups used to choose a preferred male social partner. In single male groups, where infanticide risk and paternity certainty are high, females with infants <1 year old spent more time near and affiliated more with males than females without young infants. In multi-male groups, where infanticide rates and paternity certainty are lower, mothers with new infants exhibited few behavioral changes toward males. The sole notable change was that females with young infants proportionally increased their time near males they previously spent little time near when compared to males they had previously preferred, perhaps to encourage paternity uncertainty and deter aggression. Rank was a much better predictor of females' social partner choice than paternity. Older infants (2-3 years) in multi-male groups mirrored their mothers' preferences for individual male social partners; 89% spent the most time in close proximity to the male their mother had spent the most time near when they were <1 year old. Observed discrepancies between female behavior in single and multi-male groups likely reflect different levels of postpartum intersexual conflict; in groups where paternity certainty and infanticide risk are both high, male-female interests align and females behave accordingly. This highlights the importance of considering individual and group-level variation when evaluating intersexual conflict across the reproductive cycle.