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Wobber, Victoria Elizabeth

Key insights into the evolutionary origins of human social behavior can be gained via study of our closest living relatives, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Despite being equally related to humans, these two species differ importantly in aspects of their morphology, physiology, behavior, and cognition. Morphological comparisons reveal numerous traits in bonobos that can be viewed as paedomorphic, or juvenile, relative to chimpanzees. Meanwhile, comparisons of endocrinology in the two species suggest that aspects of steroid physiology have changed significantly in bonobos in line with their reductions in male mating competition. Based on this evidence, I tested the hypothesis that behavioral and cognitive differences between bonobos and chimpanzees derive from changes in their 1) developmental trajectories of behavioral and cognitive traits and 2) neuroendocrine influences on behavior and cognition. I tested this hypothesis by studying semi free-ranging populations of bonobos and chimpanzees. First, I found that bonobos retained juvenile levels of food sharing and social inhibition into adulthood, leading them to differ from chimpanzees in these traits as adults. Second, I found that bonobos showed muted elevations in their levels of testosterone from infancy to adulthood in comparison to chimpanzees, suggesting that numerous aspects of development differ between these two species. Third, I found that male bonobos and chimpanzees differ in their immediate neuroendocrine shifts surrounding competition, implicating changes in proximate mechanisms influencing social behavior between the two species. Fourth, I found that patterns of cognitive development in these two apes differed significantly from those of human children. These results provide substantial support for my hypothesis that phenotypic differences between bonobos and chimpanzees evolved via shifts in bonobo development and neuroendocrine physiology. More broadly, they illustrate how behavioral and cognitive evolution can occur through changes in ontogenetic trajectories and neuroendocrine mechanisms. These findings thus show the merits of integrating ultimate and proximate levels of analysis in studies of the evolution of human behavior and cognition.

Background: Facilities across Africa care for apes orphaned by the trade for "bushmeat." These facilities, called sanctuaries, provide housing for apes such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) who have been illegally taken from the wild and sold as pets. Although these circumstances are undoubtedly stressful for the apes, most individuals arrive at the sanctuaries as infants and are subsequently provided with rich physical and social environments that can facilitate the expression of species-typical behaviors. Methods and Findings: We tested whether bonobo and chimpanzee orphans living in sanctuaries show any behavioral, physiological, or cognitive abnormalities relative to other individuals in captivity as a result of the early-life stress they experience. Orphans showed lower levels of aberrant behaviors, similar levels of average cortisol, and highly similar performances on a broad battery of cognitive tests in comparisons with individuals of the same species who were either living at a zoo or were reared by their mothers at the sanctuaries. Conclusion: Taken together, these results support the rehabilitation strategy used by sanctuaries in the Pan-African Sanctuary Alliance (PASA) and suggest that the orphans we examined did not show long-term signs of stress as a result of their capture. Our findings also show that sanctuary apes are as psychologically healthy as apes in other captive settings and thus represent a valuable resource for non-invasive research.

Recent research suggests that some human-like social skills evolved in dogs (Canis familiaris) during domestication as an incidental by-product of selection for “tame” forms of behavior. It is still possible, however, that the social skills of certain dog breeds came under direct selection that led to further increases in social problem solving ability. To test this hypothesis, different breeds of domestic dogs were compared for their ability to use various human communicative behaviors to find hidden food. We found that even primitive breeds with little human contact were able to use communicative cues. Further, “working” dogs (shepherds and huskies: thought to be bred intentionally to respond to human cooperative communicative signals) were more skilled at using gestural cues than were non-working breeds (basenji and toy poodles: not thought to have been bred for their cooperative-communicative ability). This difference in performance existed regardless of whether the working breeds were more or less genetically wolf-like. These results suggest that subsequent to initial domesticating selection giving rise to cue-following skills, additional selection on communicative abilities in certain breeds has produced substantive differences in those breeds’ abilities to follow cues.

Phenotypic changes between species can occur when evolution shapes development. Here, we tested whether differences in the social behavior and cognition of bonobos and chimpanzees derive from shifts in their ontogeny, looking at behaviors pertaining to feeding competition in particular. We found that as chimpanzees (n = 30) reached adulthood they became increasingly intolerant of sharing food, whereas as adults, bonobos (n = 24) maintained high, juvenile levels of food-related tolerance. We also investigated the ontogeny of inhibition during feeding competition. In two different tests, we found that bonobos (n = 30) exhibited developmental delays relative to chimpanzees (n = 29) in the acquisition of social inhibition, with these differences resulting in less skill among adult bonobos. The results suggest that these social and cognitive differences between two closely related species result from evolutionary changes in brain development.

As many studies of cognition and behavior involve captive animals, assessing any psychological impact of captive conditions is an important goal for comparative researchers. Ferdowsian and colleagues (2011) sought to address whether captive chimpanzees show elevated signs of psychopathology relative to wild apes. They modified a checklist of diagnostic criteria for major depression and posttraumatic stress disorder in humans, and applied these criteria to various captive and wild chimpanzee populations. We argue that measures derived from human diagnostic criteria are not a powerful tool for assessing the psychological health of nonverbal animals. In addition, we highlight certain methodological drawbacks of the specific approach used by Ferdowsian and colleagues (2011). We propose that research should (1) focus on objective behavioral criteria that account for species-typical behaviors and can be reliably identified across populations; (2) account for population differences in rearing history when comparing how current environment impacts psychological health in animals; and (3) focus on how changes in current human practices can improve the well-being of both captive and wild animals.

The cooking hypothesis proposes that a diet of cooked food was responsible for diverse morphological and behavioral changes in human evolution. However, it does not predict whether a preference for cooked food evolved before or after the control of fire. This question is important because the greater the preference shown by a raw-food-eating hominid for the properties present in cooked food, the more easily cooking should have been adopted following the control of fire. Here we use great apes to model food preferences by Paleolithic hominids. We conducted preference tests with various plant and animal foods to determine whether great apes prefer food items raw or cooked. We found that several populations of captive apes tended to prefer their food cooked, though with important exceptions. These results suggest that Paleolithic hominids would likewise have spontaneously preferred cooked food to raw, exapting a pre-existing preference for high-quality, easily chewed foods onto these cooked items. The results, therefore, challenge the hypothesis that the control of fire preceded cooking by a significant period.