Social cognition and cooperation

Flexible gaze following in rhesus monkeys

Bettle, R. & Rosati, A.G. (in press). Flexible gaze following in rhesus monkeys. Animal Cognition.

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Humans are characterized by complex social cognitive abilities that emerge early in development. Comparative studies of nonhuman primates can illuminate the evolutionary history of these social capacities. We examined the cognitive skills that rhesus monkeys (Macaca mulatta) use to follow gaze, a foundational skill in human social development. While rhesus monkeys can make inferences about others’ gaze when competing, it is unclear how they think about gaze information in other contexts. In Study 1, monkeys (n = 64) observed a demonstrator look upwards either in a barrier condition where a box was overhead so that monkeys could not see the target of her gaze, or a no barrier condition where nothing blocked her view. In Study 2, monkeys (n = 59) could approach to observe the target of the demonstrator’s gaze when the demonstrator looked behind a barrier on the ground or, in the no barrier condition, behind a window frame in the same location. Monkeys were more likely to directly look up in Study 1 if they could initially see the location where the demonstrator was looking, but they did not preferentially reorient their bodies to observe the out-of-view location when they could not see that location. In Study 2, monkeys did preferentially reorient, but at low rates. This indicates that rhesus monkeys can use social cognitive processes outside of competitive contexts to model what others can or cannot see, but may not be especially motivated to see what others look at in non-competitive contexts, as they reorient infrequently or in an inconsistent fashion. These similarities and differences between gaze-following in monkeys and children can help illuminate the evolution of human social cognition.

 

Chimpanzee cooperation is fast and independent from self-control

Rosati, A.G., DiNicola, L.M., & Buckholtz, J.W. (2018). Chimpanzee cooperation is fast and independent from self-control. Psychological Science, 29: 1832-1845.

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Large-scale cooperation is a hallmark of our species that appears unique amongst primates. Yet the evolutionary mechanisms that drove the emergence of human-like patterns of cooperation remain unclear. Studying the cognitive processes underlying cooperative behavior in apes, our closest living relatives, can help identify these mechanisms. Accordingly, we employed a novel test battery to assess the willingness of forty chimpanzees to donate resources, instrumentally help others, and punish a culpable thief. We found that chimpanzees were faster to make prosocial than selfish choices, and that more prosocial individuals made the fastest responses. Further, two measures of self-control did not predict variation in prosocial responding, and individual performance across cooperative tasks did not covary. These results show that chimpanzees and humans share key cognitive processes for cooperation, despite differences in the scope of their cooperative behaviors.

Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys

Rosati, A.G., Arre, A.M., Platt, M.L., & Santos, L.R. (2018). Developmental shifts in social cognition: socioemotional biases across the lifespan in rhesus monkeys.Behavioral Ecology and Sociobiology, 72: 63.

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Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition—a shift in socioemotional preferences—also occurs in nonhuman primates. Specifically, we experimentally measured socioemotional processing in a large population of rhesus macaques (Macaca mulatta) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socioemotional stimuli, to a positivity bias at older ages. We first assessed monkeys’ (n = 337) responses to negative socioemotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys’ (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Chimpanzee cognition and the roots of the human mind

Rosati, A.G. (2017). Chimpanzee cognition and the roots of the human mind. In: Chimpanzees and Human Evolution (M. Muller, R. Wrangham & D. Pilbeam, eds.). Cambridge: The Belknap Press of Harvard University Press, pp. 703-745.

[PDF] Abstract
The origins of the human mind have been a puzzle ever since Darwin (1871, 1872). Despite striking continuities in the behavior of humans and nonhumans, our species also exhibits a suite of abilities that diverge from the rest of the animal kingdom: we create and utilize complex technology, pass cultural knowledge from generation to generation, and cooperate across numerous and diverse contexts. Why do humans exhibit these abilities, but other animals (mostly) do not? This is a fundamental question in biology, psychology, and philosophy. This puzzle involves two main parts. The first is concerned with identifying the psychological capacities that are unique to humans. This phylogenetic question can be addressed through careful comparisons of humans and other animals to pinpoint the cognitive traits that are likely derived in our species. The second is concerned with the function of these capacities, and the context in which they arose. This evolutionary question examines why, from an ultimate perspective, we evolved these specialized capacities in the first place. Solving these puzzles poses a special challenge because it is only possible to directly measure the cognition of living animals. The bodies of extinct species leave traces in the fossil record, and even some behavioral traits exhibit well-understood relationships with physical traits—such as relationships between dentition and dietary ecology, or mating system and sexual size dimorphism. These relationships provide important benchmarks when biologists infer the behavior of extinct species. Unfortunately, cognition does not fossilize, and neither do the brains that generate cognitive abilities. Even those features of neuroanatomy that do leave some trace in the fossil record—such as brain size or particular anatomical landmarks—are often related to the kinds of complex cognitive capacities potentially unique to humans in a coarse fashion. As such, identifying derived human cognitive traits requires reconstructing the mind of the last common ancestor of chimpanzees (Pan troglodytes), bonobos (Pan paniscus), and humans (Homo sapiens). This reconstruction then can be used to infer what cognitive characteristics have changed in the human lineage.

Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not

Rosati, A. G., & Santos, L. R. (2017). Tolerant Barbary macaques maintain juvenile levels of social attention in old age, but despotic rhesus macaques do not. Animal Behaviour, 130, 199-207.

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Complex social life is thought to be a major driver of complex cognition in primates, but few studies have directly tested the relationship between a given primate species’ social system and their social cognitive skills. We experimentally compared lifespan patterns of a foundational social cognitive skill (following another’s gaze) in tolerant Barbary macaques, Macaca sylvanus, and despotic rhesus macaques, Macaca mulatta. Semi-free-ranging monkeys (N = 80 individuals from each species) followed gaze more in test trials where an actor looked up compared to control trials. However, species differed in ontogenetic trajectories: both exhibited high rates of gaze following as juveniles, but rhesus monkeys exhibited declines in social attention with age, whereas Barbary macaques did not. This pattern indicates that developmental patterns of social attention vary with social tolerance, and that diversity in social behaviour can lead to differences in social cognition across primates.

Understanding human gaze

Bettle, R., & Rosati, A. G. (2016). Understanding human gaze. In: Encyclopedia of Evolutionary Psychological Science (T. Shackelford and V. Weekes-Shackelford, eds.). Springer, pp. 1-4.

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Social attention is a foundational component of human social behavior. Our ability to detect and think about the direction of other’s gaze involves the attribution of mental states to others and scaffolds the development of other complex cognitive skills. Gaze-following is also widespread among other primates, but the cognitive mechanisms underlying gaze-sensitive behaviors appear to differ across species. Understanding the evolutionary origins of human social attention capacities can reveal the roots of our species’ unique patterns of cognition and culture.

Rhesus monkeys show human-like changes in gaze following across the lifespan

Rosati, A. G., Arre, A. M., Platt, M. L., & Santos, L. R. (2016). Rhesus monkeys show human-like changes in gaze following across the lifespan. Proceedings of the Royal Society B , 283, 20160376.

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Gaze following, or co-orienting with others, is a foundational skill for human social behaviour. The emergence of this capacity scaffolds critical human-specific abilities such as theory of mind and language. Non-human primates also follow others’ gaze, but less is known about how the cognitive mechanisms supporting this behaviour develop over the lifespan. Here we experimentally tested gaze following in 481 semi-free-ranging rhesus macaques (Macaca mulatta) ranging from infancy to old age. We found that monkeys began to follow gaze in infancy and this response peaked in the juvenile period—suggesting that younger monkeys were especially attuned to gaze information, like humans. After sexual maturity, monkeys exhibited human-like sex differences in gaze following, with adult females showing more gaze following than males. Finally, older monkeys showed reduced propensity to follow gaze, just as older humans do. In a second study (n = 80), we confirmed that macaques exhibit similar baseline rates of looking upwards in a control condition, regardless of age. Our findings indicate that—despite important differences in human and non-human primate life-history characteristics and typical social experiences—monkeys undergo robust ontogenetic shifts in gaze following across early development, adulthood and ageing that are strikingly similar to those of humans.

Capuchins punish those who have more

Leimgruber, K. L., Rosati, A. G., & Santos, L. R. (2016). Capuchins punish those who have more. Evolution and Human Behavior, 37, 236–244.

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Punishment of non-cooperators is important for the maintenance of large-scale cooperation in humans, but relatively little is known about the relationship between punishment and cooperation across phylogeny. The current study examined second-party punishment behavior in a nonhuman primate species known for its cooperative tendencies—the brown capuchin monkey (Cebus apella). We found that capuchins consistently punished a conspecific partner who gained possession of a food resource, regardless of whether the unequal distribution of this resource was intentional on the part of the partner. A non-social comparison confirmed that punishment behavior was not due to frustration, nor did punishment stem from increased emotional arousal. Instead, punishment behavior in capuchins appears to be decidedly social in nature, as monkeys only pursued punitive actions when such actions directly decreased the welfare of a recently endowed conspecific. This pattern of results is consistent with two features central to human cooperation: spite and inequity aversion, suggesting that the evolutionary origins of some human-like punitive tendencies may extend even deeper than previously thought.

 

Comparative developmental psychology: How is human cognitive development unique?

Rosati, A. G., Wobber, V., Hughes, K., & Santos, L. R. (2014). Comparative developmental psychology: How is human cognitive development unique?. Evolutionary Psychology, 12, 448-473.

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The fields of developmental and comparative psychology both seek to illuminate the roots of adult cognitive systems. Developmental studies target the emergence of adult cognitive systems over ontogenetic time, whereas comparative studies investigate the origins of human cognition in our evolutionary history. Despite the long tradition of research in both of these areas, little work has examined the intersection of the two: the study of cognitive development in a comparative perspective. In the current article, we review recent work using this comparative developmental approach to study non-human primate cognition. We argue that comparative data on the pace and pattern of cognitive development across species can address major theoretical questions in both psychology and biology. In particular, such integrative research will allow stronger biological inferences about the function of developmental change, and will be critical in addressing how humans come to acquire species-unique cognitive abilities.

Decision-making across social contexts: competition increases preferences for risk in chimpanzees and bonobos

Rosati, A. G., & Hare, B. (2012). Decision-making across social contexts: competition increases preferences for risk in chimpanzees and bonobos. Animal Behaviour, 84, 869-879.

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Context can have a powerful influence on decision-making strategies in humans. In particular, people sometimes shift their economic preferences depending on the broader social context, such as the presence of potential competitors or mating partners. Despite the important role of competition in primate conspecific interactions, as well as evidence that competitive social contexts impact primates’ social cognitive skills, there has been little study of how social context influences the strategies that nonhumans show when making decisions about the value of resources. Here we investigate the impact of social context on preferences for risk (variability in payoffs) in our two closest phylogenetic relatives, chimpanzees, Pan troglodytes, and bonobos, Pan paniscus. In a first study, we examine the impact of competition on patterns of risky choice. In a second study, we examine whether a positive play context affects risky choices. We find that (1) apes are more likely to choose the risky option when making decisions in a competitive context; and (2) the play context did not influence their risk preferences. Overall these results suggest that some types of social contexts can shift patterns of decision making in nonhuman apes, much like in humans. Comparative studies of chimpanzees and bonobos can therefore help illuminate the evolutionary processes shaping human economic behaviour.

Early social cognition: How psychological mechanism can inform models of decision-making

Warneken, F., & Rosati, A. G. (2012). Early social cognition: How psychological mechanism can inform models of decision-making. In: Evolving the Mechanisms of Decision Making: Toward a Darwinian Decision Theory, Strüngmann Forum Reports, vol. 11 (P. Hammerstein and J. R. Stevens, eds.). Cambridge, MA: MIT Press, pp. 288-289.

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Many approaches to understanding social decision-making use formalized models that account for costs and benefits to predict how individuals should choose. While these types of models are appropriate for describing social behavior at the ultimate level—accounting for the fitness consequences of different patterns of behavior—they do not necessarily reflect the proximate mechanisms used by decision-makers. We argue that a focus on psychological mechanisms is essential for understanding the causes of decision making in a social context. We particularly focus on the behavior of human children to elucidate the psychological capacities that are foundational for the developmental emergence of social decision-making in humans. In particular, we present evidence that across a wide range of contexts, young children appear to focus on the underlying psychological states of potential social partners in cooperative contexts. This suggests that many types of social decisions may be driven by intention-attribution, not explicit utility calculations. We propose that a comprehensive theory of social decision-making has to address both questions about ultimate function, as well as integrate empirical studies of the psychological instantiation of these processes. Developmental approaches are particularly informative, as they elucidate the origins of decision-making, as well as the factors that shape them into their mature form seen in adults.

The domestication hypothesis for dogs’ skills with human communication

Hare, B., Rosati, A. G., Kaminski, J., Braeuer, J., Call, J., & Tomasello, M. (2010). The domestication hypothesis for dogs’ skills with human communication: a response to Udell et al. (2008) and Wynne et al. (2008). Animal Behaviour , 79, e1-e6.

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Domestic dogs have special skills in comprehending human communicative behaviours. Dogs across a range of breeds use human communicative cues such as pointing or physical markers to find food that is hidden in one of two hiding places. Wolves, in contrast, do not readily exhibit this ability, suggesting that domestication may have shaped the expression of these skills in dogs. Recently, two papers challenge the ideas (1) that dogs outperform wolves in using human communicative gestures (Udell et al. 2008) and (2) that dogs require very limited human exposure to show initial skill in using such communicative cues (Wynne et al. 2008). To evaluate the evidence presented in these studies, we first discuss several methodological concerns that we have about the approach of Udell et al. (2008), then we reanalyse their data based on these methodological concerns. We also present a test of shelter dogs naıve to cognitive testing to examine whether it is the case that shelter dogs are less skilled at using human communicative cues than other groups of dogs. Finally, we directly rebut the critique of Wynne et al. (2008) and argue that there remains no evidence of significant differences in performance between dogs of different ages in their use of human communicative cues. We conclude that the domestication hypothesis remains the best explanation for dogs’ special skills for communicating with humans.

Primate social cognition: Thirty years after Premack and Woodruff

Rosati, A. G., Santos, L. R., & Hare, B. (2010). Primate social cognition: Thirty years after Premack and Woodruff. In: Primate Neuroethology (A. Ghazanfar and M. Platt, eds.). Oxford: Oxford University Press, pp. 117-143.

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Since Darwin declared the mind as the province of biology as well as psychology, the human intellect has been a major challenge for evolutionary biologists, with some researchers emphasizing the continuity between humans and other animals, and others emphasizing seemingly unique aspects of our psychological makeup. Research over the past ten years has revealed that at least some primates have some capability to assess the psychological states of others—while simultaneously showing striking differences between the social-cognitive capacities of humans and other primates. Here we address two aspects of primate social cognition—understanding of intentional, goal-directed action, and understanding perceptions, knowledge, and beliefs—focusing on newest comparative research since the last major reviews were written on the topic over a decade ago. We first review evidence suggesting that diverse species of primates understand the actions of others in terms of goals and intentions, and furthermore can reason about some, but probably not all, kinds of psychological states. We then examine the hypothesis that primates show their most complex social skills in competitive contexts, and suggest that inquiry into other aspects of primate social life, such as during cooperative interactions, may prove to be the next important step for experimental inquiries into primate social-cognitive skills. Finally, we examine primate social cognition in a broader evolutionary context that may allow us to better understand both primate and human cognitive skills.

 

Social cognition: from behavior-reading to mind-reading

Rosati, A. G., & Hare, B. (2010). Social cognition: from behavior-reading to mind-reading. In: The Encyclopedia of Behavioral Neuroscience, G. Koob, R. F. Thompson, & M. L. Moal (Ed.). Elsevier, pp. 263-268.

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The social world has long been thought to be a major force shaping primate cognition: the social lives of primates are thought to be sufficiently complex to have acted as a driving force in primate cognitive evolution. This basic thesis – that the sophisticated cognitive abilities of primates have evolved for a social function – has spurred experimental and theoretical investigations for over 40 years. In this article, we highlight a selection of complex behaviors that primates exhibit when interacting with others, with special attention to the cognitive mechanisms supporting those behaviors. Fundamental to the study of comparative cognition is the idea that many species may exhibit behaviors that appear similar, even though the psychology underlying those behaviors may differ across taxa. This distinction highlights the importance of thinking about primate social interactions not only in the context of behavioral evolution – the special things that primates (and humans) do – but also in terms of cognitive evolution – the special ways that primates think. We use this framework to analyze primate social behavior, and the differing psychologies underlying this behavior, in three areas: gaze-following, food competition, and mutualistic cooperation. The ultimate challenge of such analyses will be to understand why such different cognitive mechanisms have evolved across species.

Looking past the model species: diversity in gaze-following skills across primates

Rosati, A. G., & Hare, B. (2009). Looking past the model species: diversity in gaze-following skills across primates. Current Opinion in Neurobiology, 19, 45-51.

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Primates must navigate complex social landscapes in their daily lives: gathering information from and about others, competing with others for food and mates, and cooperating to obtain rewards as well. Gaze-following often provides important clues as to what others see, know, or will do; using information about social attention is thus crucial for primates to be competent social actors. However, the cognitive bases of the gaze-following behaviors that primates exhibit appear to vary widely across species. The ultimate challenge of such analyses will therefore be to understand why such different cognitive mechanisms have evolved across species.