Selective and Contagious Prosocial Resource Donation in Capuchin Monkeys, Chimpanzees and Humans

Prosocial acts benefitting others are widespread amongst humans. By contrast, chimpanzees have failed to demonstrate such a disposition in several studies, leading some authors to conclude that the forms of prosociality studied evolved in humans since our common ancestry. However, similar prosocial behavior has since been documented in other primates, such as capuchin monkeys. Here, applying the same methodology to humans, chimpanzees, and capuchins, we provide evidence that all three species will display prosocial behavior, but only in certain conditions. Fundamental forms of prosociality were age-dependent in children, conditional on self-beneficial resource distributions even at age seven, and conditional on social or resource configurations in chimpanzees and capuchins. We provide the first evidence that experience of conspecific companions’ prosocial behavior facilitates prosocial behavior in children and chimpanzees. Prosocial actions were manifested in all three species following rules of contingency that may reflect strategically adaptive responses

The evolution of self-control

This work was supported by the National Evolutionary Synthesis Center (NESCent) through support of a working group led by C.L.N. and B.H. NESCent is supported by the National Science Foundation (NSF) EF-0905606. For training in phylogenetic comparative methods, we thank the AnthroTree Workshop (supported by NSF BCS-0923791). Y.S. thanks the National Natural Science Foundation of China (Project 31170995) and National Basic Research Program (973 Program: 2010CB833904). E.E.B. thanks the Duke Vertical Integration Program and the Duke Undergraduate Research Support Office. J.M.P. was supported by a Newton International Fellowship from the Royal Society and the British Academy. L.R.S. thanks the James S. McDonnell Foundation for Award 220020242. L.J.N.B. and M.L.P. acknowledge the National Institutes of Mental Health (R01-MH096875 and R01-MH089484), a Duke Institute for Brain Sciences Incubator Award (to M.L.P.), and a Duke Center for Interdisciplinary Decision Sciences Fellowship (to L.J.N.B.). E.V. and E.A. thank the Programma Nazionale per la Ricerca–Consiglio Nazionale delle Ricerche (CNR) Aging Program 2012–2014 for financial support, Roma Capitale–Museo Civico di Zoologia and Fondazione Bioparco for hosting the Istituto di Scienze e Tecnologie della Cognizione–CNR Unit of Cognitive Primatology and Primate Centre, and Massimiliano Bianchi and Simone Catarinacci for assistance with capuchin monkeys. K.F. thanks the Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research 20220004. F. Aureli thanks the Stages in the Evolution and Development of Sign Use project (Contract 012-984 NESTPathfinder) and the Integrating Cooperation Research Across Europe project (Contract 043318), both funded by the European Community’s Sixth Framework Programme (FP6/2002–2006). F. Amici was supported by Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID 1138999). L.F.J. and M.M.D. acknowledge NSF Electrical, Communications, and Cyber Systems Grant 1028319 (to L.F.J.) and an NSF Graduate Fellowship (to M.M.D.). C.H. thanks Grant-in-Aid for JSPS Fellows (10J04395). A.T. thanks Research Fellowships of the JSPS for Young Scientists (21264). F.R. and Z.V. acknowledge Austrian Science Fund (FWF) Project P21244-B17, the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 311870 (to F.R.), Vienna Science and Technology Fund Project CS11-026 (to Z.V.), and many private sponsors, including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. S.M.R. thanks the Natural Sciences and Engineering Research Council (Canada). J.K.Y. thanks the US Department of Agriculture–Wildlife Services–National Wildlife Research Center. J.F.C. thanks the James S. McDonnell Foundation and Alfred P. Sloan Foundation. E.L.M. and B.H. thank the Duke Lemur Center and acknowledge National Institutes of Health Grant 5 R03 HD070649-02 and NSF Grants DGE-1106401, NSF-BCS-27552, and NSF-BCS-25172. This is Publication 1265 of the Duke Lemur Center.Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.PostprintPeer reviewe

Social interactions in wild black-fronted titi monkeys (Callicebus nigrifrons)

Social species live in groups that vary in size and composition for many reasons, including resource availability, predation risk, and space restrictions. Their social interactions reflect intraspecific interactions, social bonding, rank, reproductive status, and relatedness. Titi monkeys (Callicebus, Cheracebus, and Plecturocebus) are a diverse group of pitheciid primates that are widely distributed throughout South America. Typically, they live in small groups composed of a breeding pair and their offspring. Although social structure and interactions have been studied in captive titi monkeys, there has been much less research on free-ranging groups. We used all occurrence sampling during a 16-month period to investigate group composition and within-group social interactions in five wild groups of black-fronted titi monkeys, Callicebus nigrifrons living in an Atlantic Forest fragment at the Caraça Private Natural Heritage Reserve in Minas Gerais, Brazil. Unusually for the species, we found more than one adult male in three of our study groups (three adult males in one group and two in the other two groups). As reported for other titi monkeys, the breeding pair interacted more with each other than with any other group members. We also observed that breeding males interacted more with their offspring than breeding females did. Our results expand the existing literature on the social structure of titi monkeys, demonstrating their flexible social organization, providing further evidence of the breeding pair as the nucleus of the group and showing evidence for strong paternal care and stable attachments between breeding pairs in free-ranging C. nigrifrons

Intuitive probabilistic inference in capuchin monkeys

The ability to reason about probabilities has ecological relevance for many species. Recent research has shown that both preverbal infants and non-human great apes can make predictions about single-item samples randomly drawn from populations by reasoning about proportions. To further explore the evolutionary origins of this ability, we conducted the first investigation of probabilistic inference in a monkey species (capuchins; Sapajus spp.). Across four experiments, capuchins (N = 19) were presented with two populations of food items that differed in their relative distribution of preferred and non-preferred items, such that one population was more likely to yield a preferred item. In each trial, capuchins had to select between hidden single-item samples randomly drawn from each population. In Experiment 1 each population was homogeneous so reasoning about proportions was not required; Experiments 2–3 replicated previous probabilistic reasoning research with infants and apes; and Experiment 4 was a novel condition untested in other species, providing an important extension to previous work. Results revealed that at least some capuchins were able to make probabilistic inferences via reasoning about proportions as opposed to simpler quantity heuristics. Performance was relatively poor in Experiment 4, so the possibility remains that capuchins may use quantity-based heuristics in some situations, though further work is required to confirm this. Interestingly, performance was not at ceiling in Experiment 1, which did not involve reasoning about proportions, but did involve sampling. This suggests that the sampling task posed demands in addition to reasoning about proportions, possibly related to inhibitory control, working memory, and/or knowledge of object permanence

Diffusion dynamics of socially learned foraging techniques in squirrel monkeys

Social network analyses [1-5] and experimental studies of social learning [6-10] have each become important domains of animal behavior research in recent years yet have remained largely separate. Here we bring them together, providing the first demonstration of how social networks may shape the diffusion of socially learned foraging techniques [11]. One technique for opening an artificial fruit was seeded in the dominant male of a group of squirrel monkeys and an alternative technique in the dominant male of a second group. We show that the two techniques spread preferentially in the groups in which they were initially seeded and that this process was influenced by monkeys' association patterns. Eigenvector centrality predicted both the speed with which an individual would first succeed in opening the artificial fruit and the probability that they would acquire the cultural variant seeded in their group. These findings demonstrate a positive role of social networks in determining how a new foraging technique diffuses through a population

The role of anointing in robust capuchin monkey, Sapajus apella, social dynamics

International audienceAnointing is a behaviour in which animals apply pungent-smelling materials over their bodies. It can be done individually or socially in contact with others. Social anointing can provide coverage of body parts inaccessible to the individual, consistent with hypotheses that propose medicinal benefits. However, in highly social capuchin monkeys, Sapajus and Cebus spp., anointing has been suggested to also benefit group members through 'social bonding'. To test this, we used social network analysis to measure changes in proximity patterns during and shortly after anointing compared to a baseline condition. We presented two capuchin groups with varying quantities of onion, which reliably induces anointing, to create 'rare resource' and 'abundant resource' conditions. We examined the immediate and overall effects of anointing behaviour on the monkeys' social networks, using patterns of proximity as a measure of social bonds. For one group, proximity increased significantly after anointing over baseline values for both rare and abundant resource conditions, but for the other group proximity only increased following the rare resource condition, suggesting a role in mediating social relationships. Social interactions were affected differently in the two groups, reflecting the complex nature of capuchin social organization. Although peripheral males anointed in proximity to other group members, the weak centrality only changed in one group following anointing bouts, indicating variable social responses to anointing. We suggest in part that anointing in capuchins is analogous to social grooming: both behaviours have an antiparasitic function and can be done individually or socially requiring contact between two or more individuals. We propose that they have evolved a social function within complex repertoires of social behaviours. Our alternative perspective avoids treating medicinal and social explanations as alternative hypotheses and, along with increasing support for the medical explanations for anointing, allows us to conceptualize social anointing in capuchins as 'social medication'