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.

Insights into the evolution of social systems and species from baboon studies.

Baboons, members of the genus Papio, comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.

Flexible usage and social function in primate vocalizations.

Vocalizations are a pervasive feature of nonhuman primate social life, yet we know surprisingly little about their function. We review studies supporting the hypothesis that many primate vocalizations function to facilitate social interactions by reducing uncertainty about the signaler's intentions and likely behavior. Such interactions help to establish and maintain the social bonds that increase reproductive success. Compared with humans, songbirds, and a few other mammals, primates have small vocal repertoires that show little acoustic modification during development. However, their ability to modify call usage is extensive and tuned to variation in the social context, including the historical relationship between caller and listener and the caller's assessment of how a listener is likely to respond. We suggest parallels between the decision to vocalize and neurophysiological studies of other, nonvocal social decisions between interacting monkeys. The selective factors driving the early stages of language evolution may have come from the need to make decisions about when and how to call within the context of social challenges.

Effects of maternal investment, temperament, and cognition on guide dog success.

A continuing debate in studies of social development in both humans and other animals is the extent to which early life experiences affect adult behavior. Also unclear are the relative contributions of cognitive skills ("intelligence") and temperament for successful outcomes. Guide dogs are particularly suited to research on these questions. To succeed as a guide dog, individuals must accomplish complex navigation and decision making without succumbing to distractions and unforeseen obstacles. Faced with these rigorous demands, only ∼70% of dogs that enter training ultimately achieve success. What predicts success as a guide dog? To address these questions, we followed 98 puppies from birth to adulthood. We found that high levels of overall maternal behavior were linked with a higher likelihood of program failure. Furthermore, mothers whose nursing style required greater effort by puppies were more likely to produce successful offspring, whereas mothers whose nursing style required less effort were more likely to produce offspring that failed. In young adults, an inability to solve a multistep task quickly, compounded with high levels of perseveration during the task, was associated with failure. Young adults that were released from the program also appeared more anxious, as indicated by a short latency to vocalize when faced with a novel object task. Our results suggest that both maternal nursing behavior and individual traits of cognition and temperament are associated with guide dog success.

Temperament and problem solving in a population of adolescent guide dogs.

It is often assumed that measures of temperament within individuals are more correlated to one another than to measures of problem solving. However, the exact relationship between temperament and problem-solving tasks remains unclear because large-scale studies have typically focused on each independently. To explore this relationship, we tested 119 prospective adolescent guide dogs on a battery of 11 temperament and problem-solving tasks. We then summarized the data using both confirmatory factor analysis and exploratory principal components analysis. Results of confirmatory analysis revealed that a priori separation of tests as measuring either temperament or problem solving led to weak results, poor model fit, some construct validity, and no predictive validity. In contrast, results of exploratory analysis were best summarized by principal components that mixed temperament and problem-solving traits. These components had both construct and predictive validity (i.e., association with success in the guide dog training program). We conclude that there is complex interplay between tasks of "temperament" and "problem solving" and that the study of both together will be more informative than approaches that consider either in isolation.

Characterizing Early Maternal Style in a Population of Guide Dogs.

In both humans and non-humans, differences in maternal style during the first few weeks of life can be reliably characterized, and these differences affect offspring's temperament and cognition in later life. Drawing on the breeding population of dogs at The Seeing Eye, a guide dog school in Morristown, New Jersey, we conducted videotaped focal follows on 21 mothers and their litters (n = 138 puppies) over the first 3 weeks of the puppies' lives in an effort to characterize maternal style. We found that a mother's attitude and actions toward her offspring varied naturally between individuals, and that these variations could be summarized by a single principal component, which we described as Maternal behavior. This component was stable across weeks, associated with breed, litter size, and parity, but not redundant with these attributes. Furthermore, this component was significantly associated with an independent experimental measure of maternal behavior, and with maternal stress as measured by salivary cortisol. In summary, Maternal behavior captured a significant proportion of the variation in maternal style; was stable over time; and had both discriminant and predictive validity.

Precursors to language: Social cognition and pragmatic inference in primates.

Despite their differences, human language and the vocal communication of nonhuman primates share many features. Both constitute forms of coordinated activity, rely on many shared neural mechanisms, and involve discrete, combinatorial cognition that includes rich pragmatic inference. These common features suggest that during evolution the ancestors of all modern primates faced similar social problems and responded with similar systems of communication and cognition. When language later evolved from this common foundation, many of its distinctive features were already present.

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.

Adaptations for social cognition in the primate brain.

Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals' fitness interdependent and the 'free-rider' problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation-often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and non-social decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and non-human primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.

Long-distance communication facilitates cooperation among wild spotted hyaenas, Crocuta crocuta.

Calls that catalyse group defence, as in the mobbing of predators, appear to facilitate cooperation by recruiting receivers to act collectively. However, even when such signals reliably precede cooperative behaviour, the extent to which the calls function as recruitment signals is unclear. Calls might simply arouse listeners' attention, setting off a cascade of independent responses to the threat. By contrast, they might convey information, for example, about signaller identity and the nature of a threat that affects receivers' decisions to participate. We explored this distinction by investigating a possible long-distance recruitment call used by spotted hyaenas. These social carnivores live in fission-fusion clans and individuals disperse widely within their territories. Putative recruitment calls must therefore attract receivers that are distant from the inciting threat and free to opt out of risky collective aggression. Hyaenas compete with lions over food, and neighbouring clans sometimes engage in violent border clashes. These high-stakes contests are decided based on numerical asymmetries, so hyaenas can only protect critical resources if the dispersed clan can converge quickly at conflict sites. We recorded and analysed whoop bouts produced in multiple contexts and found that bouts produced in response to signs of lion-hyaena conflict had shorter inter-whoop intervals than spontaneous 'display' bouts. In subsequent field playback experiments, resting hyaenas were significantly more likely to move in response to 'recruitment' bouts with shortened intervals than to otherwise identical 'display' bouts. Whereas only stimulus type predicted movement, lower-ranked subjects responded most quickly, perhaps because their feeding opportunities depend on arriving early at any kill site. Results demonstrate that hyaenas possess a signal that can reliably recruit allies across long distances, despite moderating effects of individual circumstances on the strength of receivers' responses.

The costs of parental and mating effort for male baboons.

Sexual selection theory predicts that males in polygynous species of mammals will invest more reproductive effort in mate competition than parental investment. A corollary to this prediction is that males will mount a stress response when their access to mates is threatened. Indeed, numerous studies have shown that males exhibit elevated stress hormones, or glucocorticoids (GCs), when their access to females, or a proxy to this access like dominance rank, is challenged. In contrast, the relationship between stress hormones and paternal effort is less obvious. We report results from a study of wild male chacma baboons indicating that males experienced elevated GC levels during periods of social instability following the immigration of a dominant male. These effects were strongest in males whose mating opportunities were at greatest risk: high-ranking males and males engaged in sexual consortships. Males involved in friendships with lactating females, a form of paternal investment, also experienced high GC levels during these periods of instability. There was a tendency for males with lactating female friends to reduce their time spent in consortships during unstable periods, when the risk of infanticide was high. Thus, even in a highly polygynous mammal, males may have to balance paternal effort with mating effort. Males who invest entirely in mating effort risk losing the infants they have sired to infanticide. Males who invest in paternal care may enhance their offspring's survival, but at the cost of elevated GC levels, the risk of injury, and the loss of mating opportunities.

The evolution of language from social cognition.

Despite their differences, human language and the vocal communication of nonhuman primates share many features. Both constitute a form of joint action, rely on similar neural mechanisms, and involve discrete, combinatorial cognition. These shared features suggest that during evolution the ancestors of modern primates faced similar social problems and responded by evolving similar systems of perception, communication and cognition. When language later evolved from this common foundation, many of its distinctive features were already in place.

Affiliation, empathy, and the origins of theory of mind.

To understand the evolution of a Theory of Mind, we need to understand the selective factors that might have jumpstarted its initial evolution. We argue that a subconscious, reflexive appreciation of others' intentions, emotions, and perspectives is at the roots of even the most complex forms of Theory of Mind and that these abilities may have evolved because natural selection has favored individuals that are motivated to empathize with others and attend to their social interactions. These skills are adaptive because they are essential to forming strong, enduring social bonds, which in turn enhance reproductive success. We first review evidence from both humans and other animals indicating that reflexive and reflective mental state attributions are inextricably linked and play a crucial role in promoting affiliative social bonds. We next describe results from free-ranging female baboons showing that individuals who show high rates of affiliative behavior form stronger social bonds with other females. These bonds, in turn, are linked to fitness. We then provide data from three different types of social challenges (male immigration, changes in grooming behavior after the death of a close relative, and responses during playback experiments), suggesting that females who manifest high rates of affiliative behavior may also be more motivated to anticipate challenges, react adaptively to setbacks, and respond appropriately to social interactions.

Variation in personality and fitness in wild female baboons.

Studies of personality in nonhuman primates have usually relied on assessments by humans and seldom considered the function of the resulting "trait" classifications. In contrast, we applied exploratory principal component analysis to seven behaviors among 45 wild female baboons over 7 y to determine whether the personality dimensions that emerged were associated with measures of reproductive success. We identified three relatively stable personality dimensions, each characterized by a distinct suite of behaviors that were not redundant with dominance rank or the availability of kin. Females scoring high on the "Nice" dimension were friendly to all females and often grunted to lower-ranking females to signal benign intent. "Aloof" females were aggressive, less friendly, and grunted primarily to higher-ranking females. "Loner" females were often alone, relatively unfriendly, and also grunted most often to higher-ranking females. Aloof and Loner females were rarely approached by others. Personality dimensions were correlated in different ways with three measures previously shown to be associated with fitness: stress levels and two behavioral indices reflecting the closeness of dyadic bonds formed by individuals. Females who scored high on Nice had high composite sociality indices (CSI) and stable partner preferences, whereas females who scored high on Aloof had lower CSI scores but significantly more stable partner preferences. Loner females had significantly lower CSI scores, less stable partner preferences, and significantly higher glucocorticoid levels. It remains to be determined which of the Nice or Aloof personality dimensions is more adaptive, or whether variation is maintained by contrasting effects on fitness.

Animal cognition: chimpanzee alarm calls depend on what others know.

After a wild chimpanzee encounters a model of a dangerous snake, whether or not he gives an alarm call depends on his perception of another individual's knowledge.

The evolutionary origins of friendship.

Convergent evidence from many species reveals the evolutionary origins of human friendship. In horses, elephants, hyenas, dolphins, monkeys, and chimpanzees, some individuals form friendships that last for years. Bonds occur among females, among males, or between males and females. Genetic relatedness affects friendships. In species where males disperse, friendships are more likely among females. If females disperse, friendships are more likely among males. Not all friendships, however, depend on kinship; many are formed between unrelated individuals. Friendships often involve cooperative interactions that are separated in time. They depend, at least in part, on the memory and emotions associated with past interactions. Applying the term "friendship" to animals is not anthropomorphic: Many studies have shown that the animals themselves recognize others' relationships. Friendships are adaptive. Male allies have superior competitive ability and improved reproductive success; females with the strongest, most enduring friendships experience less stress, higher infant survival, and live longer.

Stability of partner choice among female baboons.

In a wide range of taxa, including baboons, close social bonds seem to help animals cope with stress and enhance long-term reproductive success and longevity. Current evidence suggests that female baboons may benefit from establishing and maintaining highly individuated relationships with a relatively small number of partners. Here, we extend previous work on the stability of female baboons' social relationships in three different ways. First, we assess the stability of females' social relationships in two distinct and geographically distant sites using the same method. Second, we conduct simulations to determine whether females' social relationships were more stable than expected by chance. Third, we examine demographic sources of variance in the stability of close social bonds. At both sites, females' relationships with their most preferred partners were significantly more stable than expected by chance. In contrast, their relationships with less preferred partners were more ephemeral, often changing from year to year. While nearly all females experienced some change in their top partners across time, many maintained relationships with top partners for several years. Females that lived in smaller groups and had more close kin available had more stable social relationships than those that lived in larger groups and had fewer close kin available.

Evidence for intra-sexual selection in wild female baboons.

Because female reproductive success in social mammals is determined largely by parental rather than mating effort, intra-sexual competition among females has typically been assumed to occur primarily over food. Recently, however, renewed attention has been paid to the importance of other sources of variation in female fitness, with a concomitant focus on a broader definition of intra-sexual selection that encompasses both competition for resources and competition for mates and social partners. We present behavioural and demographic data gathered over 15 years on a group of wild chacma baboons (Papio hamadryas ursinus) which show that females incur several costs when living in groups with many females and comparatively few males: increased intra-sexual aggression, less stable bonds with female partners, and increased mortality. Female-female aggression was higher in years when the adult sex ratio was more highly skewed toward females, with low-ranking female exhibiting particularly high rates of aggression toward other females. Females' social bonds with other females also became less stable in years when the group contained many females. Finally, female mortality rates were highest in years when the group contained comparatively more females and fewer males. The negative correlation between the number of males and female mortality suggests that the increase in mortality was due to increased predation rather than food competition. Results indicate that intra-sexual competition for social partners, mates, paternal investment, and perhaps also male protection occurs even in species where females exhibit low reproductive skew.