Differences in the early cognitive development of children and great apes.

There is very little research comparing great ape and human cognition developmentally. In the current studies we compared a cross-sectional sample of 2- to 4-year-old human children (n=48) with a large sample of chimpanzees and bonobos in the same age range (n=42, hereafter: apes) on a broad array of cognitive tasks. We then followed a group of juvenile apes (n=44) longitudinally over 3 years to track their cognitive development in greater detail. In skills of physical cognition (space, causality, quantities), children and apes performed comparably at 2 years of age, but by 4 years of age children were more advanced (whereas apes stayed at their 2-year-old performance levels). In skills of social cognition (communication, social learning, theory of mind), children out-performed apes already at 2 years, and increased this difference even more by 4 years. Patterns of development differed more between children and apes in the social domain than the physical domain, with support for these patterns present in both the cross-sectional and longitudinal ape data sets. These results indicate key differences in the pattern and pace of cognitive development between humans and other apes, particularly in the early emergence of specific social cognitive capacities in humans.

Differential changes in steroid hormones before competition in bonobos and chimpanzees.

A large body of research has demonstrated that variation in competitive behavior across species and individuals is linked to variation in physiology. In particular, rapid changes in testosterone and cortisol during competition differ according to an individual's or species' psychological and behavioral responses to competition. This suggests that among pairs of species in which there are behavioral differences in competition, there should also be differences in the endocrine shifts surrounding competition. We tested this hypothesis by presenting humans' closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus), with a dyadic food competition and measuring their salivary testosterone and cortisol levels. Given that chimpanzees and bonobos differ markedly in their food-sharing behavior, we predicted that they would differ in their rapid endocrine shifts. We found that in both species, males showed an anticipatory decrease (relative to baseline) in steroids when placed with a partner in a situation in which the two individuals shared food, and an anticipatory increase when placed with a partner in a situation in which the dominant individual obtained more food. The species differed, however, in terms of which hormone was affected; in bonobo males the shifts occurred in cortisol, whereas in chimpanzee males the shifts occurred in testosterone. Thus, in anticipation of an identical competition, bonobo and chimpanzee males showed differential endocrine shifts, perhaps due to differences in perception of the situation, that is, viewing the event either as a stressor or a dominance contest. In turn, common selection pressures in human evolution may have acted on the psychology and the endocrinology of our competitive behavior.

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.

Puberty as a life history transition.

BACKGROUND: James Tanner's landmark publication, Growth at Adolescence, was not only the first and most comprehensive treatise on the subject of human pubertal development of its time, its core insights have held up remarkably well over time. REVIEW: This review connects Tanner's contributions to contemporary understanding of puberty as a process fundamentally driven by neuroendocrine maturation. It introduces the concepts of the 'hour-glass of puberty' and 'somatic strategy' as heuristic constructs. The 'hour-glass of puberty' describes the converging pathways of information flow influencing the timing of the neuroendocrine events of puberty and its ramifying consequences throughout the body. Somatic strategy refers to the pattern of sex-specific, adult body morphology that develops at puberty as the individual undergoes a life history transition from juvenile to adult.

Bonobos have a more human-like second-to-fourth finger length ratio (2D:4D) than chimpanzees: a hypothesized indication of lower prenatal androgens.

The ratio of the second-to-fourth finger lengths (2D:4D) has been proposed as an indicator of prenatal sex differentiation. However, 2D:4D has not been studied in the closest living human relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). We report the results from 79 chimpanzees and 39 bonobos of both sexes, including infants, juveniles, and adults. We observed the expected sex difference in 2D:4D, and substantially higher, more human-like, 2D:4D in bonobos than chimpanzees. Previous research indicates that sex differences in 2D:4D result from differences in prenatal sex hormone levels. We hypothesize that the species difference in 2D:4D between bonobos and chimpanzees suggests a possible role for early exposure to sex hormones in the development of behavioral differences between the two species.

Great apes' (Pan troglodytes, Pan paniscus, Gorilla gorilla, Pongo pygmaeus) understanding of tool functional properties after limited experience.

Primates' understanding of tool functionality has been investigated extensively using a paradigm in which subjects are presented with a tool that they must use to obtain an out-of-reach reward. After being given experience on an initial problem, monkeys can transfer their skill to tools of different shapes while ignoring irrelevant tool changes (e.g., color). In contrast, monkeys without initial training perform poorly on the same tasks. Compared to most monkeys, great apes show a clear propensity for tool using and may not require as much experience to succeed on tool functionality tasks. We investigated this question by presenting 171 apes (Pan troglodytes, Pan paniscus, Gorilla gorilla, and Pongo pygmaeus) with several tool-use problems without giving them initial training or familiarizing them with the test materials. Apes succeeded without experience, but only on problems based on basic properties such as the reward being supported by an object. However, only minimal experience was sufficient to allow them to quickly improve their performance on more complex problems in which the reward was not in contact with the tool.

Autonomy in chimpanzees.

Literature on the mental capacities and cognitive mechanisms of the great apes has been silent about whether they can act autonomously. This paper provides a philosophical theory of autonomy supported by psychological studies of the cognitive mechanisms that underlie chimpanzee behavior to argue that chimpanzees can act autonomously even though their psychological mechanisms differ from those of humans. Chimpanzees satisfy the two basic conditions of autonomy: (1) liberty (the absence of controlling influences) and (2) agency (self-initiated intentional action), each of which is specified here in terms of conditions of understanding, intention, and self-control. In this account, chimpanzees make knowledge-based choices reflecting a richly information-based and socially sophisticated understanding of the world. Finally, two major theories of autonomy (Kantian theory and two-level theory) are rejected as too narrow to adequately address these issues, necessitating the modifications made in the present approach.

Comparative developmental psychology: how is human cognitive development unique?

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.

Different ontogenetic patterns of testosterone production reflect divergent male reproductive strategies in chimpanzees and bonobos.

Male reproductive effort is often strongly related to levels of the steroid hormone testosterone. However, little research has examined whether levels of testosterone throughout development might be tied to individual or species differences in the reproductive strategies pursued by adult males. Here, we tested the hypothesis that inter-specific differences in male reproductive strategy are associated with differences in the pattern of testosterone production throughout early life and puberty. We compared testosterone levels from infancy to adulthood in two closely related species where levels of mating competition and male-male aggression differ significantly, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We predicted that the reduction in male mating competition found in bonobos would be accompanied by a lesser developmental increase in testosterone production. We performed radioimmunoassay of salivary testosterone levels in a mixed-longitudinal sample of both species, collected from individuals living in semi free-ranging populations. This allowed us to examine the effects of development in a more naturalistic setting than possible in a zoo or laboratory. We found that among chimpanzees, testosterone levels declined slightly from infancy to juvenility, then remained low until increasing markedly during adolescence (with pubertal increases most pronounced among males). In contrast, there was little change in testosterone production with age in bonobos of either sex, with levels of testosterone consistent throughout infancy, juvenility, and the transition to adulthood. Our data are therefore consistent with the hypothesis that the ontogenetic pattern of testosterone production can be subject to rapid evolutionary change, shifting in association with species differences in male reproductive strategy.

Assessing the psychological health of captive and wild apes: a response to Ferdowsian et al. (2011).

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.

Psychological health of orphan bonobos and chimpanzees in African sanctuaries.

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.

Application of the heterochrony framework to the study of behavior and cognition.

Heterochrony, or the evolution of ontogeny, has been well studied in embryology and skeletal development, providing insight into morphological and genetic mechanisms of evolution.1-5 However, heterochronic studies of behavior and cognition lag behind in comparison. In a recent study we investigated the ontogeny of social behavior and cognition in humans' closest living relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). These two species are estimated to have had a chimpanzeelike common ancestor between 0.86 and 1.8 mya.6,7 Bonobos have been argued to exhibit morphological indications of paedomorphism relative to chimpanzees, especially in the cranium, and to exhibit paedomorphic behavior as adults.6-11 We found that bonobos exhibit developmental delays relative to chimpanzees in several aspects of their social behavior and cognition. Here, we describe how placing these results in the framework of heterochrony contributes to understanding behavioral and cognitive differences between adults of these two species and to our knowledge of hominid evolution in general.

Bonobos exhibit delayed development of social behavior and cognition relative to chimpanzees.

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 adult bonobos (n = 24) maintained high, juvenile levels of food-related tolerance. We also investigated the ontogeny of inhibition during tasks that simulated 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.

Testing the social dog hypothesis: are dogs also more skilled than chimpanzees in non-communicative social tasks?

Relative to non-human primates, domestic dogs possess a number of social skills that seem exceptional-particularly in solving problems involving cooperation and communication with humans. However, the degree to which dogs' unusual skills are contextually specialized is still unclear. Here, we presented dogs with a social problem that did not require them to use cooperative-communicative cues and compared their performance to that of chimpanzees to assess the extent of dogs' capabilities relative to those of non-human primates. We tested the abilities of dogs and chimpanzees to inhibit previously learned responses by using a social and a non-social version of a reversal learning task. In contrast to previous findings in cooperative-communicative social tasks, dogs were not more skilled on the social task than the non-social task, while chimpanzees were significantly better in the social paradigm. Chimpanzees were able to inhibit their prior learning better and more quickly in the social paradigm than they were in the non-social paradigm, while dogs took more time to inhibit what they had learned in both versions of the task. These results suggest that the dogs' sophisticated social skills in using human social cues may be relatively specialized as a result of domestication.

Great apes prefer cooked food.

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.