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.

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.

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.

Contingent cooperation between wild female baboons.

The apparent rarity of contingent cooperation in animals has convinced many investigators that such reciprocity is unimportant, stimulating consideration of alternative explanations for cooperation, such as by-product mutualism and biological markets motivated by the likelihood of immediate reward. Nevertheless, there is also limited evidence that animals do sometimes rely on memory of recent interactions when behaving altruistically toward others. Here we describe a playback experiment conducted on wild female baboons, suggesting that contingent cooperation may occur among unrelated individuals, even when there is a temporal delay between the two cooperative acts. Hearing the recruitment call of an unrelated recent grooming partner caused subjects to move in the direction of the loudspeaker and approach their former partner, particularly when this partner had an infant. When the subject and her partner were close kin no such effect was observed. Subjects' responses were not influenced by any type of recent interaction, because prior grooming and prior aggression influenced their behavior in qualitatively different ways. Similarly, their responses were not prompted only by the motivation to resume friendly interactions, because prior grooming alone did not elicit approach. Instead, subjects were most likely to approach their former grooming partner when they had also heard her recruitment call. Results suggest that at least some forms of cooperation in animals may be based on memory of specific recent interactions.

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.

Comparing responses of four ungulate species to playbacks of baboon alarm calls.

A growing body of evidence suggests that a wide range of animals can recognize and respond appropriately to calls produced by other species. Social learning has been implicated as a possible mechanism by which heterospecific call recognition might develop. To examine whether familiarity and/or shared vulnerability with the calling species might influence the ability of sympatric species to distinguish heterospecific alarm calls, we tested whether four ungulate species (impala: Aepyceros melampus; tsessebe: Damaliscus lunatus; zebra: Equus burchelli; wildebeest: Connochaetes taurinus) could distinguish baboon (Papio hamadryas ursinus) alarm calls from other loud baboon calls produced during intra-specific aggressive interactions ('contest' calls). Overall, subjects' responses were stronger following playback of alarm calls than contest calls. Of the species tested, impala showed the strongest responses and the greatest difference in composite response scores, suggesting they were best able to differentiate call types. Compared with the other ungulate species, impala are the most frequent associates of baboons. Moreover, like baboons, they are susceptible to both lion and leopard attacks, whereas leopards rarely take the larger ungulates. Although it seems possible that high rates of association and/or shared vulnerability may influence impala's greater ability to distinguish among baboon call types, our results point to a stronger influence of familiarity. Ours is the first study to compare such abilities among several community members with variable natural histories, and we discuss future experiments that would more systematically examine development of these skills in young ungulates.

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.

Testosterone related to age and life-history stages in male baboons and geladas.

Despite significant advances in our knowledge of how testosterone mediates life-history trade-offs, this research has primarily focused on seasonal taxa. We know comparatively little about the relationship between testosterone and life-history stages for non-seasonally breeding species. Here we examine testosterone profiles across the life span of males from three non-seasonally breeding primates: yellow baboons (Papio cynocephalus or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or P. h. ursinus), and geladas (Theropithecus gelada). First, we predict that testosterone profiles will track the reproductive profiles of each taxon across their respective breeding years. Second, we evaluate age-related changes in testosterone to determine whether several life-history transitions are associated with these changes. Subjects include males (>2.5 years) from wild populations of each taxon from whom we had fecal samples for hormone determination. Although testosterone profiles across taxa were broadly similar, considerable variability was found in the timing of two major changes: (1) the attainment of adult levels of testosterone and (2) the decline in testosterone after the period of maximum production. Attainment of adult testosterone levels was delayed by 1 year in chacmas compared with yellows and geladas. With respect to the decline in testosterone, geladas and chacmas exhibited a significant drop after 3 years of maximum production, while yellows declined so gradually that no significant annual drop was ever detected. For both yellows and chacmas, increases in testosterone production preceded elevations in social dominance rank. We discuss these differences in the context of ecological and behavioral differences exhibited by these taxa.

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.

Focused grooming networks and stress alleviation in wild female baboons.

We examine the relationship between glucocorticoid (GC) levels and grooming behavior in wild female baboons during a period of instability in the alpha male rank position. All females' GC levels rose significantly at the onset of the unstable period, though levels in females who were at lower risk of infanticide began to decrease sooner in the following weeks. Three factors suggest that females relied on a focused grooming network as a coping mechanism to alleviate stress. First, all females' grooming networks became less diverse in the weeks following the initial upheaval. Second, females whose grooming had already focused on a few predictable partners showed a less dramatic rise in GC levels than females whose grooming network had been more diverse. Third, females who contracted their grooming network the most experienced a greater decrease in GC levels in the following week. We conclude that close bonds with a few preferred partners allow female baboons to alleviate the stress associated with social instability.

Kin-mediated reconciliation substitutes for direct reconciliation in female baboons.

It has been hypothesized that group-living mammals engage in reconciliation (post-conflict affiliation between former opponents) to reduce the disruptive costs of aggression and restore opponents' tolerance to baseline levels. Recipients of aggression are sometimes reluctant to tolerate the proximity of a recent opponent, however, in apparent fear that aggression will be renewed. In such cases, reconciliatory behaviour by the aggressor's close kin may substitute for direct reconciliation. We describe a playback experiment with free-ranging baboons (Papio hamadryas ursinus) that examines whether friendly behaviour by the aggressor's kin can substitute for direct reconciliation by the aggressor herself. In the test condition, female subjects who had recently been threatened heard the friendly grunt of one of their aggressor's relatives, mimicking kin-mediated vocal reconciliation. In the control condition, subjects heard the grunt of a dominant female from a different matriline. Subjects responded significantly more strongly in test than in control trials. Moreover, in the next hour they were significantly more likely to tolerate the proximity of both their aggressor and the relative whose grunt they had heard. In contrast, subjects' behaviour towards both control females and other members of their aggressor's matriline was unaffected. We conclude that kin-mediated vocal reconciliation can substitute for direct reconciliation in baboons.

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.

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.

Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus).

In humans, bereavement is associated with an increase in glucocorticoid (GC) levels, though this increase can be mitigated by social support. We examined faecal GC levels and grooming behaviour of free-ranging female baboons to determine whether similar effects were also evident in a non-human species. Females who lost a close relative experienced a significant increase in GC levels in the weeks following their relative's death compared with the weeks before, whereas control females showed no such increase. Despite the fact that females concentrate much of their grooming on close kin, females who lost a close female relative did not experience a decrease in grooming rate and number of grooming partners; instead, both grooming rate and number of grooming partners increased after a relative's death. While the death of a close relative was clearly stressful over the short term, females appeared to compensate for this loss by broadening and strengthening their grooming networks. Perhaps as a result, females' GC levels soon returned to baseline. Even in the presence of familiar troop-mates and other relatives, females experienced a stress response when they lost specific companions, and they apparently sought to alleviate it by broadening and strengthening their social relationships.

Primate social cognition and the origins of language.

Are the cognitive mechanisms underlying language unique, or can similar mechanisms be found in other domains? Recent field experiments demonstrate that baboons' knowledge of their companions' social relationships is based on discrete-valued traits (identity, rank, kinship) that are combined to create a representation of social relations that is hierarchically structured, open-ended, rule-governed, and independent of sensory modality. The mechanisms underlying language might have evolved from the social knowledge of our pre-linguistic primate ancestors.