Federica Amici

The Evolution of Self-Control

Significance Although scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problem-solving tasks measuring self-control and evaluated the leading hypotheses regarding how and why cognition evolves. Across species, differences in absolute (not relative) brain volume best predicted performance on these tasks. Within primates, dietary breadth also predicted cognitive performance, whereas social group size did not. These results suggest that increases in absolute brain size provided the biological foundation for evolutionary increases in self-control, and implicate species differences in feeding ecology as a potential selective pressure favoring these skills. 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.

The evolutionary origin of human hyper-cooperation

Proactive, that is, unsolicited, prosociality is a key component of our hyper-cooperation, which in turn has enabled the emergence of various uniquely human traits, including complex cognition, morality and cumulative culture and technology. However, the evolutionary foundation of the human prosocial sentiment remains poorly understood, largely because primate data from numerous, often incommensurable testing paradigms do not provide an adequate basis for formal tests of the various functional hypotheses. We therefore present the results of standardized prosociality experiments in 24 groups of 15 primate species, including humans. Extensive allomaternal care is by far the best predictor of interspecific variation in proactive prosociality. Proactive prosocial motivations therefore systematically arise whenever selection favours the evolution of cooperative breeding. Because the human data fit this general primate pattern, the adoption of cooperative breeding by our hominin ancestors also provides the most parsimonious explanation for the origin of human hyper-cooperation.

Monkeys and apes: are their cognitive skills really so different?

Differences in cognitive skills across taxa, and between monkeys and apes in particular, have been explained by different hypotheses, although these often are not supported by systematic interspecific comparisons. Here, we directly compared the cognitive performance of the four great apes and three monkey species (spider monkeys, capuchin monkeys, and long-tailed macaques), differing in their phylogenetic-relatedness and socioecology. We tested subjects on their ability to remember object locations (memory task), track object displacements (transposition task), and obtain out-of-reach rewards (support task). Our results showed no support for an overall clear-cut distinction in cognitive skills between monkeys and apes as species performance varied substantially across tasks. Although we found differences in performance at tracking object displacements between monkeys and apes, interspecific differences in the other two tasks were better explained in terms of differential socioecology, especially differential levels of fission-fusion dynamics. A cluster analysis using mean scores of each condition of the three tasks for each species suggested that the only dichotomy might be between members of the genus Pan and the rest of the tested species. These findings evidence the importance of using multiple tasks across multiple species in a comparative perspective to test different explanations for the enhancement of specific cognitive skills.

Lack of prosociality in great apes, capuchin monkeys and spider monkeys: convergent evidence from two different food distribution tasks

Prosociality can be defined as any behaviour performed to alleviate the needs of others or to improve their welfare. Prosociality has probably played an essential role in the evolution of cooperative behaviour and several studies have already investigated it in primates to understand the evolutionary origins of human prosociality. Two main tasks have been used to test prosociality in a food context. In the Platforms task, subjects can prosocially provide food to a partner by selecting a prosocial platform over a selfish one. In the Tokens task, subjects can prosocially provide food to a partner by selecting a prosocial token over a selfish one. As these tasks have provided mixed results, we used both tasks to test prosociality in great apes, capuchin monkeys and spider monkeys. Our results provided no compelling evidence of prosociality in a food context in any of the species tested. Additionally, our study revealed serious limitations of the Tokens task as it has been previously used. These results highlight the importance of controlling for confounding variables and of using multiple tasks to address inconsistencies present in the literature.

A modular mind? A test using individual data from seven primate species

It has long been debated whether the mind consists of specialized and independently evolving modules, or whether and to what extent a general factor accounts for the variance in performance across different cognitive domains. In this study, we used a hierarchical Bayesian model to re-analyse individual level data collected on seven primate species (chimpanzees, bonobos, orangutans, gorillas, spider monkeys, brown capuchin monkeys and long-tailed macaques) across 17 tasks within four domains (inhibition, memory, transposition and support). Our modelling approach evidenced the existence of both a domain-specific factor and a species factor, each accounting for the same amount (17%) of the observed variance. In contrast, inter-individual differences played a minimal role. These results support the hypothesis that the mind of primates is (at least partially) modular, with domain-specific cognitive skills undergoing different evolutionary pressures in different species in response to specific ecological and social demands.

Sex Differences in the Development of Social Relationships in Rhesus Macaques (Macaca mulatta)

Several studies have documented the importance of social bonding for the enhancement of individual fitness. However, little is known about how social relationships develop through ontogeny, and whether their development follows the same trajectory in males and females. Here we analyzed affiliative interactions (proximity, social grooming, play) combined with demographic and genetic data in semi-free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago over their first 4 yr of life (from birth to sexual maturation) to understand how these interactions change through development in both sexes. Generalized linear mixed models revealed that social behaviors mostly followed different developmental trajectories in males and females and were highly dependent on the social context. In particular, sex differences in social behavior varied through development depending on the partner’s sex and age. Females engaged in more social interactions than males, especially with other females, and were more involved in grooming around the time of maturation. In contrast, males interacted more with males and age peers, especially around maturation. Sex differences in social behavior varied through development, but also depended on rank, partner’s rank, and kin line, although not consistently. High-ranking individuals, especially older females, were generally preferred as social partners. Moreover, both male and female individuals interacted mostly with maternal kin, although males also preferred paternal kin over nonkin. Importantly, most developmental changes in sociality happened when individuals were ca. 2 yr old, suggesting that this might be a milestone in the development of sociality in rhesus macaques. The only notable exception to this pattern was play, which was more pronounced in males from the beginning of their lives. We propose that play might serve as a trigger of sex differences in social behavior, with sex differences emerging early in development and increasing through time as males and females gradually grow into their adult social roles.

Sex differences in the development of aggressive behavior in rhesus macaques (Macaca mulatta)

Aggressive behavior plays a central role in primate life, having a crucial effect on their reproductive performance and survival and possibly affecting the formation and maintenance of social bonds. Although aggressive behavior might serve a different function in males and females, and sex differences in aggressive behavior seem to emerge early during development, very few studies have investigated whether aggressive patterns follow different developmental trajectories in male and female primates. However, the developmental perspective is crucial to understanding when differences in adults’ aggression emerge and which factors trigger them. We here analyzed aggressive interactions in rhesus macaques from birth to sexual maturation (before male dispersal), including male and female focal subjects. We further considered the partner’s sex, age, and rank, as well as maternal and paternal kinship, and used powerful multivariate statistical analysis. The probability to initiate aggression was largely similar for both sexes and throughout development. Both males and females were more aggressive toward partners of the same sex and similar age. In contrast, the probability of receiving aggression mostly differed between sexes across development and depended on the social context. The probability of receiving aggression increased through development. Finally, important developmental changes appeared between 2 and 3 yr of age, indicating that this period is crucial for the development of adult social roles. Our results suggest that aggressive behavior largely serves a similar function for both sexes during the first years of development, only partially anticipating adult aggressive patterns.

Calculated reciprocity? A comparative test with six primate species

Little evidence of calculated reciprocity has been found in non-human primates so far. In this study, we used a simple experimental set-up to test whether partners pulled a sliding table to altruistically provide food to each other in short-term interactions. We tested 46 dyads of chimpanzees, bonobos, gorillas, orangutans, brown capuchin monkeys and spider monkeys to examine whether a subject’s tendency to provide food to a partner was directly affected by the partner’s previous behaviour, by the species, by the condition (i.e., whether the partner could access the food provided by the subject) and by the social tolerance levels within each dyad. Chimpanzees and orangutans were the only species pulling significantly more when the partner could retrieve the food altruistically provided. However, no species reciprocated food exchanges, as subjects’ probability to pull was not affected by the previous number of the partner’s pulls, with the possible exception of one orangutan dyad. Although subjects clearly knew how the apparatus worked and easily obtained food for themselves, individuals did not usually take the opportunity to provide food to their partners, suggesting that calculated reciprocity is not a common behaviour and that food exchanges are usually not reciprocated in the short-term within dyads.

Response facilitation in the four great apes : Is there a role for empathy?

Contagious yawning is a form of response facilitation found in humans and other primates in which observing a model yawning enhances the chance that the observer will also yawn. Because contagious yawning seems to be more easily triggered when models are conspecifics or have a strong social bond with the observer, it has been proposed that contagious yawning is linked to empathy. A possible way to test this hypothesis is to analyze whether individuals’ responses differ when they observe models yawning or performing different involuntary (i.e., nose wiping, scratching) and voluntary (i.e., hand closing, wrist shaking) actions that are not linked to empathy. In this study, we tested the four great ape species with two different setups by exposing them to a human experimenter repeatedly performing these actions online, and video-recorded conspecifics repeatedly performing these actions on a screen. We examined which behaviors were subject to response facilitation, whether response facilitation was triggered by both human models and video-recorded conspecifics, and whether all species showed evidence of response facilitation. Our results showed that chimpanzees yawned significantly more when and shortly after watching videos of conspecifics (but not humans) yawning than in control conditions, and they did not do so as a response to increased levels of anxiety. For all other behaviors, no species produced more target actions when being exposed to either model than under control conditions. Moreover, the individuals that were more “reactive” when watching yawning videos were not more reactive when exposed to other actions. Since, at least in chimpanzees, (1) subjects only showed response facilitation when they were exposed to yawning and (2) only if models were conspecifics, it appears that contagious yawning is triggered by unique mechanisms and might be linked to empathy.

Aversion to violation of expectations of food distribution: the role of social tolerance and relative dominance in seven primate species

Studies on how animals behave when two partners receive different amounts of food have produced variable results, with individuals responding negatively to specific food distributions in some cases (e.g., when food is distributed unequally between partners), but not in others. In this study, we used a simple experimental approach to (i) assess the strictness of dominance relationships based on the degree of social tolerance and (ii) compare the behavioural responses of seven primate species (chimpanzees, Pan troglodytes; bonobos, Pan paniscus; gorillas, Gorilla gorilla; orangutans, Pongo pygmaeus; brown capuchin monkeys, Cebus apella; spider monkeys, Ateles geoffroyi; long-tailed macaques, Macaca fascicularis), when two partners received different amounts of food and no effort was required. We predicted that negative responses (i.e., refusal to participate in the task or avoidance of proximity to the food source) would be elicited by food distributions that violate the individual expectations based on tolerance levels and subject’s dominance rank relative to the partner. In the ‘tolerance’ task, we found that species with less strict dominance relationships were chimpanzees and bonobos, followed by orangutans, spider monkeys, gorillas, brown capuchin monkeys and long-tailed macaques. In the ‘food distribution’ task, capuchin monkeys and especially macaques showed their aversion by refusing to participate in most conditions, including the ones with equal food distribution. When dominants received more food than the partner, subjects of all species maintained a comparable amount of proximity to the food source, possibly reflecting the general acceptance of such a food distribution across species. When dominants received less than or as much as their partners, dominant capuchin monkeys maintained less proximity than other species, possibly because having different expectations of food distributions (i.e., more/all food to the dominant). Our study highlights the importance of the species’ degree of social tolerance and the relative dominance rank between partners in the study of violation of expectations of different food distributions.