Evolutionary variation

Chimpanzees and bonobos exhibit emotional reactions to decision outcomes

Rosati, A. G., & Hare, B. (2013). Chimpanzees and bonobos exhibit emotional reactions to decision outcomes. PLoS One, 8 e63058.

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The interface between cognition, emotion, and motivation is thought to be of central importance in understanding complex cognitive functions such as decision-making and executive control in humans. Although nonhuman apes have complex repertoires of emotional expression, little is known about the role of affective processes in ape decision-making. To illuminate the evolutionary origins of human-like patterns of choice, we investigated decision-making in humans’ closest phylogenetic relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). In two studies, we examined these species’ temporal and risk preferences, and assessed whether apes show emotional and motivational responses in decision making contexts. We find that (1) chimpanzees are more patient and more risk-prone than are bonobos, (2) both species exhibit affective and motivational responses following the outcomes of their decisions, and (3) some emotional and motivational responses map onto species-level and individual-differences in decision-making. These results indicate that apes do exhibit emotional responses to decision-making, like humans. We explore the hypothesis that affective and motivational biases may underlie the psychological mechanisms supporting value-based preferences in these species.

Chimpanzees and bonobos exhibit divergent spatial memory development

Rosati, A. G., & Hare, B. (2012). Chimpanzees and bonobos exhibit divergent spatial memory development. Developmental Science, 15, 840-853.

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Spatial cognition and memory are critical cognitive skills underlying foraging behaviors for all primates. While the emergence of these skills has been the focus of much research on human children, little is known about ontogenetic patterns shaping spatial cognition in other species. Comparative developmental studies of nonhuman apes can illuminate which aspects of human spatial development are shared with other primates, versus which aspects are unique to our lineage. Here we present three studies examining spatial memory development in our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (P. paniscus). We first compared memory in a naturalistic foraging task where apes had to recall the location of resources hidden in a large outdoor enclosure with a variety of landmarks (studies 1 and 2). We then compared older apes using a matched memory choice paradigm (study 3). We found that chimpanzees exhibited more accurate spatial memory than bonobos across contexts, supporting predictions from these species’ different feeding ecologies. Furthermore, chimpanzees—but not bonobos—showed developmental improvements in spatial memory, indicating that bonobos exhibit cognitive paedomorphism (delays in developmental timing) in their spatial abilities relative to chimpanzees. Together, these results indicate that the development of spatial memory may differ even between closely related species. Moreover, changes in the spatial domain can emerge during nonhuman ape ontogeny, much like some changes seen in human children.

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.

How does cognition evolve? Phylogenetic comparative psychology.

MacLean, E., Matthews, L. J., Hare, B., Nunn, et al. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15, 223-238.

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Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Chimpanzees and bonobos distinguish between risk and ambiguity

Rosati, A. G., & Hare, B. (2011). Chimpanzees and bonobos distinguish between risk and ambiguity. Biology Letters, 7 15-18.

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Although recent research has investigated animal decision-making under risk, little is known about how animals choose under conditions of ambiguity when they lack information about the available alternatives. Many models of choice behaviour assume that ambiguity does not impact decision-makers, but studies of humans suggest that people tend to be more averse to choosing ambiguous options than risky options with known probabilities. To illuminate the evolutionary roots of human economic behaviour, we examined whether our closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), share this bias against ambiguity. Apes chose between a certain option that reliably provided an intermediately preferred food type, and a variable option that could vary in the probability that it provided a highly preferred food type. To examine the impact of ambiguity on ape decision-making, we interspersed trials in which chimpanzees and bonobos had no knowledge about the probabilities. Both species avoided the ambiguous option compared with their choices for a risky option, indicating that ambiguity aversion is shared by humans, bonobos and chimpanzees.

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.

The adaptive nature of context-dependent choice

Rosati, A. G., & Stevens, J. R. (2009). The adaptive nature of context-dependent choice. In: Rational Animal, Irrational Human, S. Watanabe, A. Young, A. Blaisdell, & Y. Yamazaki (Ed.). Tokyo, Keio University Press, pp. 101-117.

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Although classical economic theory hinges on the assumption that rational actors should seek to maximize gains, psychologists and behavioral economists have recently collected a wealth of evidence challenging this premise. In violation of the principles of rational choice, context appears to dramatically influence human decision making. Like humans, numerous nonhuman animals, ranging from honeybees to primates, are sensitive to context, suggesting deep evolutionary roots for seemingly irrational decision-making. Many psychologists have suggested that such choices may stem from cognitive biases that result in errors. We contend, however, that labeling context-dependent choices as errors obscures the real issue. Natural selection does not create organisms that adhere to economic theory—it creates decision makers that maximize fitness. We review evidence that many species show context-dependence when making decisions and then present a framework for analyzing the adaptive consequences of these choices. We argue for an approach weaving psychological perspectives into an evolutionary framework to elucidate the nature of decision making.

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.

A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos

Heilbronner, S. R., Rosati, A. G., Stevens, J. R., Hare, B., & Hauser, M. D. (2008). A fruit in the hand or two in the bush? Divergent risk preferences in chimpanzees and bonobos. Biology Letters, 4, 246-249.

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Human and non-human animals tend to avoid risky prospects. If such patterns of economic choice are adaptive, risk preferences should reflect the typical decision-making environments faced by organisms. However, this approach has not been widely used to examine the risk sensitivity in closely related species with different ecologies. Here, we experimentally examined risk-sensitive behaviour in chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), closely related species whose distinct ecologies are thought to be the major selective force shaping their unique behavioural repertoires. Because chimpanzees exploit riskier food sources in the wild, we predicted that they would exhibit greater tolerance for risk in choices about food. Results confirmed this prediction: chimpanzees significantly preferred the risky option, whereas bonobos preferred the fixed option. These results provide a relatively rare example of risk-prone behaviour in the context of gains and show how ecological pressures can sculpt economic decision making.

The evolutionary origins of human patience: Temporal preferences in chimpanzees, bonobos, and human adults

Rosati, A. G., Stevens, J. R., Hare, B., & Hauser, M. D. (2007). The evolutionary origins of human patience: Temporal preferences in chimpanzees, bonobos, and human adults. Current Biology, 17, 1663–1668.

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To make adaptive choices, individuals must sometimes exhibit patience, forgoing immediate benefits to acquire more valuable future rewards. Although humans account for future consequences when making temporal decisions, many animal species wait only a few seconds for delayed benefits. Current research thus suggests a phylogenetic gap between patient humans and impulsive, present-oriented animals, a distinction with implications for our understanding of economic decision making and the origins of human cooperation. On the basis of a series of experimental results, we reject this conclusion. First, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) exhibit a degree of patience not seen in other animals tested thus far. Second, humans are less willing to wait for food rewards than are chimpanzees. Third, humans are more willing to wait for monetary rewards than for food, and show the highest degree of patience only in response to decisions about money involving low opportunity costs. These findings suggest that core components of the capacity for future-oriented decisions evolved before the human lineage diverged from apes. Moreover, the different levels of patience that humans exhibit might be driven by fundamental differences in the mechanisms representing biological versus abstract rewards.

The effect of handling time on temporal discounting in two New World primates

Rosati, A. G., Stevens, J. R., & Hauser, M. D. (2006). The effect of handling time on temporal discounting in two New World primates. Animal Behaviour, 71, 1379-1387.

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Foraging decisions in nonhuman animals often require choosing between small, immediate food rewards and larger, more delayed rewards. Faced with such choices, animals typically discount or devalue the future quite strongly. Although discounting studies often focus on delays to reward access, other temporal intervals contribute to foraging rate, and thus may potentially influence discounting levels. Here, we examine the effect of handling time, the time required to process and consume food, on discounting in cottontop tamarins, Saguinus oedipus, and common marmosets, Callithrix jacchus, two species that differ in levels of temporal discounting. We presented subjects with a discounting task under two conditions. In the first condition, we made the entire reward available after the delay expired. In the second condition, we experimentally increased the minimum length of time required to consume the reward to simulate a longer handling time. We found that tamarins and marmosets showed sensitivity to increases in the time necessary to process food rewards. Both species adjusted their preferences to account for different handling times at long delays to accessing food. Consequently, models of discounting behaviour that include handling times may better describe animal choices than models that focus exclusively on delays prior to access.

Means-means-end tool choice in cotton-top tamarins

Santos, L. R., Rosati, A. G., Spaulding, B., Sproul, C., & Hauser, M. D. (2005). Means-means-end tool choice in cotton-top tamarins (Sanguinus oedipus): finding the limits on primates’ knowledge of tools. Animal Cognition, 8, 236-246.

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Most studies of animal tool use require subjects to use one object to gain access to a food reward. In many real world situations, however, animals perform more than one action in sequence to achieve their goals. Of theoretical interest is whether animals have the cognitive capacity to recognize the relationship between consecutive action sequences in which there may be one overall goal and several subgoals. Here we ask if cotton-top tamarins, a species that in captivity uses tools to solve means-end problems, can go one step further and use a sequence of tools (means) to obtain food (end). We first trained subjects to use a pulling tool to obtain a food reward. After this initial training, subjects were presented with problems in which one tool had to be used in combination with a second in order to obtain food. Subjects showed great difficulty when two tools were required to obtain the food reward. Although subjects attended to the connection between the tool and food reward, they ignored the physical connection between the two tools. After training on a two-tool problem, we presented subjects with a series of transfer tests to explore if they would generalize to new types of connections between the tools. Subjects readily transferred to new connections. Our results therefore provide the first evidence to date that tamarins can learn to solve problems involving two tools, but that they do so only with sufficient training.

Will travel for food: Spatial discounting in two New World monkeys

Stevens, J. R., Rosati, A. G., Ross, K. R., & Hauser, M. D. (2005). Will travel for food: Spatial discounting in two New World monkeys. Current Biology, 15, 1855–1860.

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Nonhuman animals steeply discount the future, showing a preference for small, immediate over large, delayed rewards. Currently unclear is whether discounting functions depend on context. Here, we examine the effects of spatial context on discounting in cotton-top tamarins (Saguinus oedipus) and common marmosets (Callithrix jacchus), species known to differ in temporal discounting. We presented subjects with a choice between small, nearby rewards and large, distant rewards. Tamarins traveled farther for the large reward than marmosets, attending to the ratio of reward differences rather than their absolute values. This species difference contrasts with performance on a temporal task in which marmosets waited longer than tamarins for the large reward. These comparative data indicate that context influences choice behavior, with the strongest effect seen in marmosets who discounted more steeply over space than over time. These findings parallel details of each species’ feeding ecology. Tamarins range over large distances and feed primarily on insects, which requires using quick, impulsive action. Marmosets range over shorter distances than tamarins and feed primarily on tree exudates, a clumped resource that requires patience to wait for sap to exude. These results show that discounting functions are context specific, shaped by a history of ecological pressures.