Gestural communication in olive baboons (Papio anubis): repertoire and intentionality.

Gesturing is a widespread phenomenon in the animal kingdom, as well as an important facet of human language. As such, studying the communicative gestures of our close phylogenetic relatives is essential to better understand its evolution. While recent studies have shown that ape gestural communication shares some properties with human language, very little is known about the properties of gestural communication in monkeys. The aims of this study were to establish the first quantitative repertoire of gestural communication in a species of old-world monkeys, the olive baboon Papio anubis, and to determine its properties in terms of variability, flexibility, and intentionality. Gestural communication was continuously recorded on 47 captive olive baboons over 1 year. Their gestural repertoire was composed of 67 visual, tactile, and audible gestures, which were used flexibly across different contexts, indicating means-ends dissociation. We found that the use of gestures was variable across individuals and ages, notably with repertoire size decreasing with age. Baboons used their gestures intentionally; gesturers looked at the recipient, waited for a response, and took into account the attentional state of their recipient. Particularly, they actively adjusted the modality of their gesture to the recipient's visual attention, using more visual gestures when the recipient was attending and more tactile gestures when the recipient was not. Thus, the gestural communicative system of olive baboons possesses properties which are similar to the ones of apes and to human language. These intentional features of gestural communication, that may constitute a prerequisite of language evolution, may have been present in the common ancestor of baboons and humans, around 30-40 million years ago.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure.

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher-order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely-related species. We use a social network approach to describe higher-order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species-typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex-ratio, and current living condition (captive vs. free-living). We assembled 34-38 datasets of female-female dyadic aggression and allogrooming among captive and free-living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newman's modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate-strong phylogenetic signals in dominance traits, but moderate-weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely-connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Evidence of direct reciprocity, but not of indirect and generalized reciprocity, in the grooming exchanges of wild Barbary macaques (Macaca sylvanus).

Reciprocity is one of the mechanisms that have been proposed to explain the exchange of social behaviors, such as grooming, in animals. Reciprocity assumes that individuals act as the donor and recipient of grooming and switch roles over time to balance the benefits and costs of this behavior. Three main patterns of reciprocity may follow a grooming given: (i) direct reciprocity, where the former recipient returns the grooming to the former donor; (ii) indirect reciprocity, where another individual returns the grooming to the former donor; and (iii) generalized reciprocity, where the former recipient returns the grooming to another individual. While there is evidence that direct reciprocity plays an important role in various species of animals, the role of indirect and generalized reciprocity is less clear and has been rarely analyzed. We tested the role of direct, indirect, and generalized reciprocity in explaining grooming exchanges of wild Barbary macaques, by analyzing the temporal contingency between giving and receiving grooming. We collected the occurrence and latency of the three types of grooming reciprocation during 1 hr long focal sessions run simultaneously on two partners who just stopped grooming (post-grooming session) or who were in proximity (i.e., within 1.5 m) without grooming each other (control session). We ran the analyses on 284 post-grooming and 63 control sessions. The results revealed a temporal contingency of grooming interactions exchanged according to direct reciprocity but not according to indirect or generalized reciprocity. Our results indicate that grooming distribution in Barbary macaques is partner-specific. We discuss the possible role of cognition and emotions in explaining direct reciprocity in animals.

Cooperation in wild Barbary macaques: factors affecting free partner choice.

A key aspect of cooperation is partner choice: choosing the best available partner improves the chances of a successful cooperative interaction and decreases the likelihood of being exploited. However, in studies on cooperation subjects are rarely allowed to freely choose their partners. Group-living animals live in a complex social environment where they can choose among several social partners differing in, for example, sex, age, temperament, or dominance status. Our study investigated whether wild Barbary macaques succeed to cooperate using an experimental apparatus, and whether individual and social factors affect their choice of partners and the degree of cooperation. We used the string pulling task that requires two monkeys to manipulate simultaneously a rope in order to receive a food reward. The monkeys were free to interact with the apparatus or not and to choose their partner. The results showed that Barbary macaques are able to pair up with a partner to cooperate using the apparatus. High level of tolerance between monkeys was necessary for the initiation of successful cooperation, while strong social bond positively affected the maintenance of cooperative interactions. Dominance status, sex, age, and temperament of the subjects also affected their choice and performance. These factors thus need to be taken into account in cooperative experiment on animals. Tolerance between social partners is likely to be a prerequisite for the evolution of cooperation.

Is Conceptual Diversity an Advantage for Scientific Inquiry? A Case Study on the Concept of 'Gesture' in Comparative Psychology.

Growing scientific fields often involve multidisciplinary investigations in which the same concepts may have different meanings. Here, we examine the case of 'gesture' in comparative research to depict how conceptual diversity hidden by the label 'gesture' can lead to consistently divergent interpretations in humans and nonhuman primates. We show that definitions of 'gesture' drastically differ regarding the forms of a gesture and the cognitive processes inferred from it, and that these differences emerge from implicit assumptions which have pervasive consequences on the interpretations claimed by researchers. We then demonstrate that implicit assumptions about scientific concepts can be made explicit using a finite set of operational criteria. We argue that developing theoretical definitions systematically associated with operational conceptual boundaries would allow to tackle both the challenges of maintaining high internal coherence within studies and of improving comparability and replicability of scientific results. We thus offer an easy-to-implement conceptual tool that should help ground valid comparisons between studies and serve scientific inquiry.

Handedness in monkeys reflects hemispheric specialization within the central sulcus. An in vivo MRI study in right- and left-handed olive baboons.

Handedness, one of the most prominent expressions of laterality, has been historically considered unique to human. This noteworthy feature relates to contralateral inter-hemispheric asymmetries in the motor hand area following the mid-portion of the central sulcus. However, within an evolutionary approach, it remains debatable whether hand preferences in nonhuman primates are associated with similar patterns of hemispheric specialization. In the present study conducted in Old world monkeys, we investigate anatomical asymmetries of the central sulcus in a sample of 86 olive baboons (Papio anubis) from in vivo T1 anatomical magnetic resonance images (MRI). Out of this sample, 35 individuals were classified as right-handed and 28 as left-handed according to their hand use responses elicited by a bimanual coordinated tube task. Here we report that the direction and degree of hand preference (left or right), as measured by this manual task, relates to and correlates with contralateral hemispheric sulcus depth asymmetry, within a mid-portion of the central sulcus. This neuroanatomical manifestation of handedness in baboons located in a region, which may correspond to the motor hand area, questions the phylogenetic origins of human handedness that may date back to their common ancestor, 25-40 millions years ago.

Hand preferences for unimanual and bimanual coordinated actions in olive baboons (Papio anubis): Consistency over time and across populations.

The reliability of handedness data in nonhuman primates and variations of sample size across studies are critical issues for exploring their potential continuity with humans concerning hemispheric specialization. In this study, we investigated the consistency of handedness for unimanual and bimanual tasks in olive baboons (Papio anubis). For both tasks, we found a consistency of hand preferences over time among subjects retested 5 years later and a consistency of population-level handedness between 2 independent populations. Altogether, when combining the 2 samples, bimanual (N = 260) but not unimanual task (N = 220) elicited right-handedness predominance. These findings demonstrate the reliability and robustness of predominance of right-handedness in olive baboons for bimanual coordinated behaviors. (PsycINFO Database Record

Right-handedness predominance in 162 baboons (Papio anubis) for gestural communication: consistency across time and groups.

Whether nonhuman primates exhibit population level right manual bias remains a controversial topic. In captive baboons, population-level right-handedness has been reported for both coordinated bimanual actions and communicative gestures. However, some authors remain skeptical of these findings on both methodological and theoretical grounds. Here, we demonstrated the robustness and the consistency across time of the pattern of right-handedness for a species-specific communicative gesture in olive baboons (Papio anubis). First, we showed significant correlations in the 26 retested baboons for the measures of hand preferences between the first and the second session conducted 4 years later (2005-2009) by an observer blind to the previous handedness data. Second, the replication of the study in 96 novel individuals revealed a similar degree of population-level right-handedness than the one expressed in the first group of 66 subjects investigated in 2005. The implications of the findings are discussed within a theoretical framework about the origin of hemispheric specialization for language.