Accelerated reproduction is not an adaptive response to early-life adversity in wild baboons.

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.

Social bonds do not mediate the relationship between early adversity and adult glucocorticoids in wild baboons.

In humans and other animals, harsh conditions in early life can have profound effects on adult physiology, including the stress response. This relationship may be mediated by a lack of supportive relationships in adulthood. That is, early life adversity may inhibit the formation of supportive social ties, and weak social support is itself often linked to dysregulated stress responses. Here, we use prospective, longitudinal data from wild baboons in Kenya to test the links between early adversity, adult social bonds, and adult fecal glucocorticoid hormone concentrations (a measure of hypothalamic-pituitary-adrenal [HPA] axis activation and the stress response). Using a causal inference framework, we found that experiencing one or more sources of early adversity led to a 9 to 14% increase in females' glucocorticoid concentrations across adulthood. However, these effects were not mediated by weak social bonds: The direct effects of early adversity on adult glucocorticoid concentrations were 11 times stronger than the effects mediated by social bonds. This pattern occurred, in part, because the effect of social bonds on glucocorticoids was weak compared to the powerful effects of early adversity on glucocorticoid levels in adulthood. Hence, in female baboons, weak social bonds in adulthood are not enough to explain the effects of early adversity on glucocorticoid concentrations. Together, our results support the well-established notions that early adversity and weak social bonds both predict poor adult health. However, the magnitudes of these two effects differ considerably, and they may act independently of one another.

Philopatry at the frontier: A demographically driven scenario for the evolution of multilevel societies in baboons (Papio).

The baboons (Papio sp.) exhibit marked interspecies variation in social behavior. The thesis presented here argues, first, that male philopatry is a crucial factor, arguably the crucial factor, underlying the other distinctive features (one-male units, multilevel society) shared by hamadryas and Guinea baboons, but not other species of Papio. The second suggestion is that male philopatry as a population norm was not an adaptation to a particular habitat or set of ecological circumstances but evolved in the common ancestor of hamadryas and Guinea baboons as a response to natural selection in the demographic context peculiar to the frontier of a rapidly expanding population. Other derived features of social structure (male-male tolerance, some facultative female dispersal) subsequently evolved to accommodate male philopatry. The mitochondrial genetic population structure of extant baboons preserves a footprint of the initial expansion of 'modern' Papio. Immediately after the expansion, male-philopatric, multilevel populations with a general physical and behavioral resemblance to Guinea baboons occupied the whole northern hemisphere range of the genus. Behavioral and physical autapomorphies of hamadryas baboons evolved in a subpopulation of this ancestral northern base, in response to a less productive habitat of the Horn of Africa. Subsequently, ancestral olive baboons 'reinvented' male dispersal. They and yellow baboons, another male-dispersing species, then replaced most of the male-philopatric northern populations, by male-driven introgression and nuclear swamping.

On the evolution of baboon greeting rituals.

To balance the trade-offs of male co-residence, males living in multi-male groups may exchange ritualized greetings. Although these non-aggressive signals are widespread in the animal kingdom, the repertoire described in the genus Papio is exceptional, involving potentially harmful behaviours such as genital fondling. Such greetings are among the most striking male baboon social interactions, yet their function remains disputed. Drawing on the comprehensive analysis from our own research on wild Guinea baboons, combined with a survey of the literature into other baboon species, we review the form and function of male-male ritualized greetings and their relation to the various social systems present in this genus. These ritualized signals differ between species in their occurrence, form and function. While ritualized greetings are rare in species with the most intense contest competition, the complexity of and risk involved in greeting rituals increase with the degree of male-male tolerance and cooperation. The variety of societies found in this genus, combined with its role as a model for human socioecological evolution, sheds light on the evolution of ritualized behaviour in non-human primates and rituals in humans. This article is part of the theme issue 'Ritual renaissance: new insights into the most human of behaviours'.

Baboon vocal repertoires and the evolution of primate vocal diversity.

A remarkable and derived trait of humans is the faculty for language, and considerable research effort has been devoted to understanding the evolution of speech. In contrast to spoken language, which constitutes a (learned) symbolic communication system, the acoustic structure of nonhuman primate vocalizations is largely genetically fixed. Yet, appreciable differences between different genera and species may exist. Environmental conditions, sexual selection, and characteristics of the social system have been invoked to explain these differences. Here, we studied the acoustic variation of call types and vocal repertoires in the genus Papio. Because the genus comprises both stable groups as well as multi-level societies, and reveals striking variation in the degree of aggressiveness from south to north, it constitutes a promising model to assess the link between social system characteristics and vocal communication. We found that, the vocal repertoires of the different species were composed of the same general call types. A quantitative analysis of the acoustic features of the grunts and loud calls of chacma (Papio ursinus), olive (P. anubis), and Guinea (P. papio) baboons showed subtle acoustic differences within call types, however. Social system characteristics did not map onto acoustic variation. We found no correlation between the structure of grunts and geographic distance; the same was true for female loud calls. Only for male loud calls from three populations, call structure varied with geographic distance. Our findings corroborate the view that the structure of nonhuman primate vocalizations is highly conserved, despite the differences in social systems. Apparently, variation in rate and intensity of occurrence of signals, probably due to different behavioral dispositions in species, are sufficient to allow for plasticity at the level of the social relationships, mating patterns, and social organization.

Functional social structure in baboons: Modeling interactions between social and environmental structure in group-level foraging.

In mobile social groups, cohesion is thought to be driven by patterns of attraction at both the individual and group level. In long-lived species with high group stability and repeated interactions, such as baboons, individual-to-individual attractions have the potential to play a large role in group cohesion and overall movement patterns. In previous work, we found that the patterning of inter-individual attraction gave rise to an emergent group-level structure, whereby a core of more influential, inter-dependent individuals exerted a unidirectional influence on the movements of peripheral animals. Here, we use agent-based modeling of baboon groups to investigate whether this core-periphery structure has any functional consequences for foraging behavior. By varying individual level attractions, we produced baboon groups that contained influence structures that varied from more to less centralized. Our results suggest that varying centrality affects both the ability of the group to detect resource structure in the environment, as well as the ability of the group to exploit these resources. Our models predict that foraging groups with more centralized social structures will show a reduction in detection and an increase in exploitation of resources in their environment, and will produce more extreme foraging outcomes. More generally, our results highlight how a group's internal social structure can result in mobile social animals being able to more (or less) effectively exploit environmental structure, and capitalize on the distribution of resources. In addition, our agent-based model can be used to generate testable predictions that can be tested among the extant baboon allotaxa. This will add value to the existing body of work on responses to local ecology, as well as providing a means to test hypotheses relating to the phylogeography of the baboons and, by analogy, shed light on patterns of hominin evolution in time and space.

The baboon: A model for the study of language evolution.

Comparative research on the origins of human language often focuses on a limited number of language-related cognitive functions or anatomical structures that are compared across species. The underlying assumption of this approach is that a single or a limited number of factors may crucially explain how language appeared in the human lineage. Another potentially fruitful approach is to consider human language as the result of a (unique) assemblage of multiple cognitive and anatomical components, some of which are present in other species. This paper is a first step in that direction. It focuses on the baboon, a non-human primate that has been studied extensively for years, including several brain, anatomical, cognitive and cultural dimensions that are involved in human language. This paper presents recent data collected on baboons regarding (1) a selection of domain-general cognitive functions that are core functions for language, (2) vocal production, (3) gestural production and cerebral lateralization, and (4) cumulative culture. In all these domains, it shows that the baboons share with humans many cognitive or brain mechanisms which are central for language. Because of the multidimensionality of the knowledge accumulated on the baboon, that species is an excellent nonhuman primate model for the study of the evolutionary origins of language.

Group size effects on inter-blink interval as an indicator of antipredator vigilance in wild baboons.

Vigilance in animals is an important means for predator detection. Animals living in groups reduce their predation risk as more individuals are present. In contrast to most other animals studied, many studies on primates do not support the prediction that individual vigilance will decline as group size increases. For animals to obtain visual information during vigilance behaviour, their eyes must be open. Therefore, if animals are able to perceive differential risk of predation, the inter-blink interval (eye-opening) should increase, and the blink duration (eye-closure) should decrease under higher predation risk. We tested this prediction by measuring inter-blink interval in wild anubis baboons (Papio anubis) in peripheral and centre individuals within a group, and between larger and smaller groups. We found that the inter-blink interval for young males, often located at the front edge of the group, was longer than that of adult males, adult females, and young females, often located in the center of the group, and that the inter-blink interval for adult males was longer when the group was smaller. These results suggest that inter-blink interval can be used as an indicator of primate vigilance toward predators.

Individual variation in local interaction rules can explain emergent patterns of spatial organization in wild baboons.

Researchers have long noted that individuals occupy consistent spatial positions within animal groups. However, an individual's position depends not only on its own behaviour, but also on the behaviour of others. Theoretical models of collective motion suggest that global patterns of spatial assortment can arise from individual variation in local interaction rules. However, this prediction remains untested. Using high-resolution GPS tracking of members of a wild baboon troop, we identify consistent inter-individual differences in within-group spatial positioning. We then apply an algorithm that identifies what number of conspecific group members best predicts the future location of each individual (we call this the individual's neighbourhood size) while the troop is moving. We find clear variation in the most predictive neighbourhood size, and this variation relates to individuals' propensity to be found near the centre of their group. Using simulations, we show that having different neighbourhood sizes is a simple candidate mechanism capable of linking variation in local individual interaction rules-in this case how many conspecifics an individual interacts with-to global patterns of spatial organization, consistent with the patterns we observe in wild primates and a range of other organisms.

Emotion-Cognition Interaction in Nonhuman Primates: Cognitive Avoidance of Negative Stimuli in Baboons (Papio papio)

It is well established that emotion and cognition interact in humans, but such an interaction has not been extensively studied in nonhuman primates. We investigated whether emotional value can affect nonhuman primates' processing of stimuli that are only mentally represented, not visually available. In a short-term memory task, baboons memorized the location of two target squares of the same color, which were presented with a distractor of a different color. Through prior long-term conditioning, one of the two colors had acquired a negative valence. Subjects were slower and less accurate on the memory task when the targets were negative than when they were neutral. In contrast, subjects were faster and more accurate when the distractors were negative than when they were neutral. Some of these effects were modulated by individual differences in emotional disposition. Overall, the results reveal a pattern of cognitive avoidance of negative stimuli, and show that emotional value alters cognitive processing in baboons even when the stimuli are not physically present. This suggests that emotional influences on cognition are deeply rooted in evolutionary continuity.

Insights into the genetic foundation of aggression in Papio and the evolution of two length-polymorphisms in the promoter regions of serotonin-related genes (5-HTTLPR and MAOALPR) in Papionini.

BACKGROUND: Aggressive behaviors are an integral part of competitive interactions. There is considerable variation in aggressiveness among individuals both within and among species. Aggressiveness is a quantitative trait that is highly heritable. In modern humans and macaques (Macaca spp.), variation in aggressiveness among individuals is associated with polymorphisms in the serotonergic (5-HT) neurotransmitter system. To further investigate the genetics underlying interspecific variation in aggressiveness, 123 wild individuals from five baboon species (Papio papio, P. hamadryas, P. anubis, P. cynocephalus, and P. ursinus) were screened for two polymorphisms in promoter regions of genes relevant for the 5-HT system (5-HTTLPR and MAOALPR). RESULTS: Surprisingly, despite considerable interspecific variation in aggressiveness, baboons are monomorphic in 5-HTTLPR, except for P. hamadryas, which carries one additional allele. Accordingly, this locus cannot be linked to behavioral variation among species. A comparison among 19 papionin species, including nine species of macaques, shows that the most common baboon allele is similar to the one described for Barbary macaques (Macaca sylvanus), probably representing the ancestral allele in this tribe. It should be noted that (almost) all baboons live in Africa, but within Macaca only M. sylvanus lives on this continent. Baboons are, however, highly polymorphic in the so-called 'warrior gene' MAOALPR, carrying three alleles. Due to considerable variation in allele frequencies among populations of the same species, this genotype cannot be invoked to explain variation in aggressiveness at the species level. CONCLUSIONS: This study provides another indication that 5-HTTLPR is not related to aggressiveness in primates per se, but may have been under differential selective pressures among taxa and potentially among populations in different geographic regions. The results on MAOALPR alleles in Papio indicate that variation in the metabolism of monoamine neurotransmitters and associated behaviors is more important among populations than among species. We, therefore, propose to compile behavioral data from additional populations of Papio to obtain further insight into the genetics underlying behavioral differences among primate species.

Cumulative early life adversity predicts longevity in wild baboons.

In humans and other animals, harsh circumstances in early life predict morbidity and mortality in adulthood. Multiple adverse conditions are thought to be especially toxic, but this hypothesis has rarely been tested in a prospective, longitudinal framework, especially in long-lived mammals. Here we use prospective data on 196 wild female baboons to show that cumulative early adversity predicts natural adult lifespan. Females who experience ≥3 sources of early adversity die a median of 10 years earlier than females who experience ≤1 adverse circumstances (median lifespan is 18.5 years). Females who experience the most adversity are also socially isolated in adulthood, suggesting that social processes partially explain the link between early adversity and adult survival. Our results provide powerful evidence for the developmental origins of health and disease and indicate that close ties between early adversity and survival arise even in the absence of health habit and health care-related explanations.

Self-organizing dominance hierarchies in a wild primate population.

Linear dominance hierarchies, which are common in social animals, can profoundly influence access to limited resources, reproductive opportunities and health. In spite of their importance, the mechanisms that govern the dynamics of such hierarchies remain unclear. Two hypotheses explain how linear hierarchies might emerge and change over time. The 'prior attributes hypothesis' posits that individual differences in fighting ability directly determine dominance ranks. By contrast, the 'social dynamics hypothesis' posits that dominance ranks emerge from social self-organization dynamics such as winner and loser effects. While the prior attributes hypothesis is well supported in the literature, current support for the social dynamics hypothesis is limited to experimental studies that artificially eliminate or minimize individual differences in fighting abilities. Here, we present the first evidence supporting the social dynamics hypothesis in a wild population. Specifically, we test for winner and loser effects on male hierarchy dynamics in wild baboons, using a novel statistical approach based on the Elo rating method for cardinal rank assignment, which enables the detection of winner and loser effects in uncontrolled group settings. Our results demonstrate (i) the presence of winner and loser effects, and (ii) that individual susceptibility to such effects may have a genetic basis. Taken together, our results show that both social self-organization dynamics and prior attributes can combine to influence hierarchy dynamics even when agonistic interactions are strongly influenced by differences in individual attributes. We hypothesize that, despite variation in individual attributes, winner and loser effects exist (i) because these effects could be particularly beneficial when fighting abilities in other group members change over time, and (ii) because the coevolution of prior attributes and winner and loser effects maintains a balance of both effects.

Baboons' response speed is biased by their moods.

The affect-as-information hypothesis (e.g., Schwarz & Clore, 2003), predicts that the positive or negative valence of our mood differentially affects our processing of the details of the environment. However, this hypothesis has only been tested with mood induction procedures and fairly complex cognitive tasks in humans. Here, six baboons (Papio papio) living in a social group had free access to a computerized visual search task on which they were over-trained. Trials that immediately followed a spontaneously expressed emotional behavior were analyzed, ruling out possible biases due to induction procedures. RTs following negatively valenced behaviors are slower than those following neutral and positively valenced behaviors, respectively. Thus, moods affect the performance of nonhuman primates tested in highly automatized tasks, as it does in humans during tasks with much higher cognitive demands. These findings reveal a presumably universal and adaptive mechanism by which moods influence performance in various ecological contexts.

Contribution of working memory processes to relational matching-to-sample performance in baboons (Papio papio).

Recent studies of monkeys and apes have shown that these animals can solve relational-matching-to-sample (RMTS) problems, suggesting basic abilities for analogical reasoning. However, doubts remain as to the actual cognitive strategies adopted by nonhuman primates in this task. Here, we used dual-task paradigms to test 10 baboons in the RMTS problem under three conditions of memory load. Our three test conditions allowed different predictions, depending on the strategy (i.e., flat memorization of the percept, reencoding of the percept, or relational processing) that they might use to solve RMTS problems. Results support the idea that the baboons process both the items and the abstract (same and different) relations in this task.