Differences in the cognitive skills of bonobos and chimpanzees.

While bonobos and chimpanzees are both genetically and behaviorally very similar, they also differ in significant ways. Bonobos are more cautious and socially tolerant while chimpanzees are more dependent on extractive foraging, which requires tools. The similarities suggest the two species should be cognitively similar while the behavioral differences predict where the two species should differ cognitively. We compared both species on a wide range of cognitive problems testing their understanding of the physical and social world. Bonobos were more skilled at solving tasks related to theory of mind or an understanding of social causality, while chimpanzees were more skilled at tasks requiring the use of tools and an understanding of physical causality. These species differences support the role of ecological and socio-ecological pressures in shaping cognitive skills over relatively short periods of evolutionary time.

How does cognition evolve? Phylogenetic comparative psychology.

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.

Use of "entertainment" chimpanzees in commercials distorts public perception regarding their conservation status.

Chimpanzees (Pan troglodytes) are often used in movies, commercials and print advertisements with the intention of eliciting a humorous response from audiences. The portrayal of chimpanzees in unnatural, human-like situations may have a negative effect on the public's understanding of their endangered status in the wild while making them appear as suitable pets. Alternatively, media content that elicits a positive emotional response toward chimpanzees may increase the public's commitment to chimpanzee conservation. To test these competing hypotheses, participants (n = 165) watched a series of commercials in an experiment framed as a marketing study. Imbedded within the same series of commercials was one of three chimpanzee videos. Participants either watched 1) a chimpanzee conservation commercial, 2) commercials containing "entertainment" chimpanzees or 3) control footage of the natural behavior of wild chimpanzees. Results from a post-viewing questionnaire reveal that participants who watched the conservation message understood that chimpanzees were endangered and unsuitable as pets at higher levels than those viewing the control footage. Meanwhile participants watching commercials with entertainment chimpanzees showed a decrease in understanding relative to those watching the control footage. In addition, when participants were given the opportunity to donate part of their earnings from the experiment to a conservation charity, donations were least frequent in the group watching commercials with entertainment chimpanzees. Control questions show that participants did not detect the purpose of the study. These results firmly support the hypothesis that use of entertainment chimpanzees in the popular media negatively distorts the public's perception and hinders chimpanzee conservation efforts.

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

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. © 2012 The Association for the Study of Animal Behaviour.

Chimpanzees and bonobos exhibit divergent spatial memory development.

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.

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

To make adaptive choices, individuals must sometimes exhibit patience, forgoing immediate benefits to acquire more valuable future rewards [1-3]. Although humans account for future consequences when making temporal decisions [4], many animal species wait only a few seconds for delayed benefits [5-10]. Current research thus suggests a phylogenetic gap between patient humans and impulsive, present-oriented animals [9, 11], a distinction with implications for our understanding of economic decision making [12] and the origins of human cooperation [13]. 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.

Chimpanzees and bonobos distinguish between risk and ambiguity.

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.

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

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.

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.

Increasing arousal enhances inhibitory control in calm but not excitable dogs

© 2015, Springer-Verlag Berlin Heidelberg.The emotional-reactivity hypothesis proposes that problem-solving abilities can be constrained by temperament, within and across species. One way to test this hypothesis is with the predictions of the Yerkes–Dodson law. The law posits that arousal level, a component of temperament, affects problem solving in an inverted U-shaped relationship: Optimal performance is reached at intermediate levels of arousal and impeded by high and low levels. Thus, a powerful test of the emotional-reactivity hypothesis is to compare cognitive performance in dog populations that have been bred and trained based in part on their arousal levels. We therefore compared a group of pet dogs to a group of assistance dogs bred and trained for low arousal (N = 106) on a task of inhibitory control involving a detour response. Consistent with the Yerkes–Dodson law, assistance dogs, which began the test with lower levels of baseline arousal, showed improvements when arousal was artificially increased. In contrast, pet dogs, which began the test with higher levels of baseline arousal, were negatively affected when their arousal was increased. Furthermore, the dogs’ baseline levels of arousal, as measured in their rate of tail wagging, differed by population in the expected directions. Low-arousal assistance dogs showed the most inhibition in a detour task when humans eagerly encouraged them, while more highly aroused pet dogs performed worst on the same task with strong encouragement. Our findings support the hypothesis that selection on temperament can have important implications for cognitive performance.

Citizen Science as a New Tool in Dog Cognition Research.

Family dogs and dog owners offer a potentially powerful way to conduct citizen science to answer questions about animal behavior that are difficult to answer with more conventional approaches. Here we evaluate the quality of the first data on dog cognition collected by citizen scientists using the Dognition.com website. We conducted analyses to understand if data generated by over 500 citizen scientists replicates internally and in comparison to previously published findings. Half of participants participated for free while the other half paid for access. The website provided each participant a temperament questionnaire and instructions on how to conduct a series of ten cognitive tests. Participation required internet access, a dog and some common household items. Participants could record their responses on any PC, tablet or smartphone from anywhere in the world and data were retained on servers. Results from citizen scientists and their dogs replicated a number of previously described phenomena from conventional lab-based research. There was little evidence that citizen scientists manipulated their results. To illustrate the potential uses of relatively large samples of citizen science data, we then used factor analysis to examine individual differences across the cognitive tasks. The data were best explained by multiple factors in support of the hypothesis that nonhumans, including dogs, can evolve multiple cognitive domains that vary independently. This analysis suggests that in the future, citizen scientists will generate useful datasets that test hypotheses and answer questions as a complement to conventional laboratory techniques used to study dog psychology.

Social Decision-Making in Bonobos and Chimpanzees

Humans are natural politicians. We obsessively collect social information that is both observable (e.g., about third-party relationships) and unobservable (e.g., about others’ psychological states), and we strategically employ that information to manage our cooperative and competitive relationships. To what extent are these abilities unique to our species, and how did they evolve? The present dissertation seeks to contribute to these two questions. To do so, I take a comparative perspective, investigating social decision-making in humans’ closest living relatives, bonobos and chimpanzees. In Chapter 1, I review existing literature on theory of mind—or the ability to understand others’ psychological states—in these species. I also present a theoretical framework to guide further investigation of social cognition in bonobos and chimpanzees based on hypotheses about the proximate and ultimate origins of their species differences. In Chapter 2, I experimentally investigate differences in the prosocial behavior of bonobos and chimpanzees, revealing species-specific prosocial motivations that appear to be less flexible than those exhibited by humans. In Chapter 3, I explore through decision-making experiments bonobos’ ability to evaluate others based on their prosocial or antisocial behavior during third-party interactions. Bonobos do track the interactions of third-parties and evaluate actors based on these interactions. However, they do not exhibit the human preference for those who are prosocial towards others, instead consistently favoring an antisocial individual. The motivation to prefer those who demonstrate a prosocial disposition may be a unique feature of human psychology that contributes to our ultra-cooperative nature. In Chapter 4, I investigate the adaptive value of social cognition in wild primates. I show that the recruitment behavior of wild chimpanzees at Gombe National Park, Tanzania is consistent with the use of third-party knowledge, and that those who appear to use third-party knowledge receive immediate proximate benefits. They escape further aggression from their opponents. These findings directly support the social intelligence hypothesis that social cognition has evolved in response to the demands of competing with one’s own group-mates. Thus, the studies presented here help to better characterize the features of social decision-making that are unique to humans, and how these abilities evolved.

Implantation of mouse embryonic stem cell-derived cardiac progenitor cells preserves function of infarcted murine hearts.

Stem cell transplantation holds great promise for the treatment of myocardial infarction injury. We recently described the embryonic stem cell-derived cardiac progenitor cells (CPCs) capable of differentiating into cardiomyocytes, vascular endothelium, and smooth muscle. In this study, we hypothesized that transplanted CPCs will preserve function of the infarcted heart by participating in both muscle replacement and neovascularization. Differentiated CPCs formed functional electromechanical junctions with cardiomyocytes in vitro and conducted action potentials over cm-scale distances. When transplanted into infarcted mouse hearts, CPCs engrafted long-term in the infarct zone and surrounding myocardium without causing teratomas or arrhythmias. The grafted cells differentiated into cross-striated cardiomyocytes forming gap junctions with the host cells, while also contributing to neovascularization. Serial echocardiography and pressure-volume catheterization demonstrated attenuated ventricular dilatation and preserved left ventricular fractional shortening, systolic and diastolic function. Our results demonstrate that CPCs can engraft, differentiate, and preserve the functional output of the infarcted heart.