The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Development of the visual preference of chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) for photographs of primates: effect of social experience

In a study by Tanaka (2003) five captive chimpanzees preferred photographs of humans to those of chimpanzees. All the subjects were raised by humans and lived in captivity for many years. This suggests their preference might have developed through social experience. In this study examined this hypothesis by using three young chimpanzees raised by their mothers in a captive chimpanzee community. The young chimpanzees were tested four times before six years of age. I also tested eight adult chimpanzees that had been in captivity for more than 20 years. Each subject was presented with digitized color photographs of different species of primates on a touch-sensitive screen. The subjects received a food reward when they touched a photograph, irrespective of which photograph they touched. All the adult chimpanzees touched photographs of humans more frequently than those of any other species of primate. Two of the young chimpanzees showed no species preference before reaching 5 years of age, when they started to show preference for humans. The remaining young chimpanzee consistently preferred chimpanzees. These results suggest that development of visual preference of chimpanzees is affected by social experience during infancy.     

Mother-infant relations and infant development in captive chimpanzees and orang-utans

Four chimpanzee (Pan troglodytes)mother—infant dyads and four orangutan (Pongo pygmaeus)motherinfant dyads were studied for the first 11 months of the infants’ lives. For both species, ventroventral contact and nipple contact decreased over time at a similar rate, but total contact decreased earlier in the orangutans and was 50% lower than for the chimpanzees at the end of the study. Social play between the mothers and the infants did not differ in frequency between the species, but orangutans played above the ground and chimpanzees on the ground. Solitary play differed in form between the species and, like social play, reflected their differences in arboreal and terrestrial proclivities. In addition, the orangutans engaged in solitary play considerably more frequently than the chimpanzees during the second half-year of life. The developmental differences in mother-infant contact and solitary play of these apes are consistent with the differences in their speciestypical social organization. The data may reflect, therefore, early development of species differences in the social and relatively solitary natures of chimpanzees and orangutans, respectively. An erratum to this article is available at .     

灵长类社会玩耍的行为模式、影响因素及其功能风险

社会玩耍是指两个或两个以上个体共同参与的一种互作性玩耍行为,个体间的行为彼此适应并相互影响。社会玩耍行为在灵长类物种的社会交往过程中普遍发生,作为未成年个体一种重要的发育行为,其对个体的生存技能和成年后的繁殖成功具有重要影响。灵长类物种的社会玩耍不仅仅表现为追逐、摔跤、跳跃等一些常见行为,部分物种还发展出自己特有的行为。一般而言,社会玩耍在婴儿后期和青少年早期的发生频率最高,然后随着年龄增长直到成年时期,这类行为的平均发生频率将逐渐下降。未成年雄性个体要比同年龄段的雌性个体更喜欢玩耍,但常因物种、研究对象年龄等因素表现不同甚至相反;很多物种的个体喜欢与有亲缘关系的个体玩耍,或者与性别相同、年龄相仿、等级相近的个体玩耍。总之,非人灵长类个体社会玩耍的发育不但受环境参量如食物、场地等的影响,而且还与个体的年龄、性别、等级、亲缘关系等社群因素紧密相关。未成年个体在玩耍过程中,获得了身体机能的快速发育、完善了生存技能、建立了个体间的友好关系、增强了认识自身及适应周围环境的能力,从而为顺利过渡到成年期和履行自己的职能打好基础,但有时却需要承担玩耍过程中受伤甚至死亡的风险。玩耍作为灵长类社会的一种行为文化,对其研究有助于对人类自身行为进化的不断认识,相信这方面的理论将会得到后来者的不断创新和丰富,也期望这方面的理念及经验能被及时运用到保护繁育等实践活动中。     

Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain embedded in a uniquely shaped braincase. Here, we quantitatively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and unique aspects in developmental patterns of these two species can help us to understand brain evolution in the hominin lineage.Using CT scans of 58 humans and 60 chimpanzees varying in age from birth to adulthood, we generated virtual endocasts to measure and analyze 29 three-dimensional endocranial landmarks and several hundred semilandmarks on curves and the endocranial surface; these data were then analyzed using geometric morphometric methods.The ontogenetic shape trajectories are nonlinear for both species, which indicates several developmental phases. Endocranial shape is already distinct at birth and there is no overlap between the two species throughout ontogeny. While some aspects of the pattern of endocranial shape change are shared between humans and chimpanzees, the shape trajectories differ substantially directly after birth until the eruption of the deciduous dentition: in humans but not in chimpanzees, the parietal and cerebellar regions expand relatively (contributing to neurocranial globularity) and the cranial base flexes within the first postnatal year when brain growth rates are high. We show that the shape changes associated with this early “globularization phase” are unique to humans and do not occur in chimpanzees before or after birth.     

The Occurrence of Postconflict Skills in Captive Immature Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)

Conflict management strategies can reduce costs of aggressive competition in group-living animals. Postconflict behaviors such as reconciliation and third-party postconflict affiliation are widely accepted as social skills in primates and have been demonstrated in many species. Although immature primates possess a repertoire of species-specific behaviors, it is thought that they gradually develop appropriate social skills throughout prolonged juvenility to establish and maintain complex social relationships within their group. We examined the occurrence of postconflict skills in five immature chimpanzees (Pan troglodytes) over 15 mo, focusing on interactions that were not with the subject’s mother. We observed reconciliation, with conciliatory tendencies comparable to adults, and provide the first evidence that captive immature chimpanzees commonly reconciled using social play. However, immatures were not more likely to reconcile valuable than nonvaluable relationships. We also observed third party postconflict affiliation although at a lower level than reported for adults. Our results provide evidence for postconflict skills in immature chimpanzees but the lack of higher conciliatory tendency with valuable partners and low occurrence of third-party affiliation indicates extended juvenility may be required refine these skills. Further work is needed to investigate whether these behaviors have the same function and effectiveness as those found in adults.     

Differential prefrontal white matter development in chimpanzees and humans

A comparison of developmental patterns of white matter (WM) within the prefrontal region between humans and nonhuman primates is key to understanding human brain evolution. WM mediates complex cognitive processes and has reciprocal connections with posterior processing regions [1, 2]. Although the developmental pattern of prefrontal WM in macaques differs markedly from that in humans [3], this has not been explored in our closest evolutionary relative, the chimpanzee. The present longitudinal study of magnetic resonance imaging scans demonstrated that the prefrontal WM volume in chimpanzees was immature and had not reached the adult value during prepuberty, as observed in humans but not in macaques. However, the rate of prefrontal WM volume increase during infancy was slower in chimpanzees than in humans. These results suggest that a less mature and more protracted elaboration of neuronal connections in the prefrontal portion of the developing brain existed in the last common ancestor of chimpanzees and humans, and that this served to enhance the impact of postnatal experiences on neuronal connectivity. Furthermore, the rapid development of the human prefrontal WM during infancy may help the development of complex social interactions, as well as the acquisition of experience-dependent knowledge and skills to shape neuronal connectivity.     

Visual preference in a human-reared agile gibbon (<Emphasis Type="Italic">Hylobates agilis</Emphasis>)

Visual preference was evaluated in a male agile gibbon. The subject was raised by humans immediately after birth, but lived with his biological family from one year of age. Visual preference was assessed using a free-choice task in which five or six photographs of different primate species, including humans, were presented on a touch-sensitive screen. The subject touched one of them. Food rewards were delivered irrespective of the subject’s responses. We prepared two types of stimulus sets. With set 1, the subject touched photographs of humans more frequently than those of other species, recalling previous findings in human-reared chimpanzees. With set 2, photographs of nine species of gibbons were presented. Chimpanzees touched photographs of white-handed gibbons more than those of other gibbon species. The gibbon subject initially touched photographs of agile gibbons more than white-handed gibbons, but after one and two years his choice patterns resembled the chimpanzees’. The results suggest that, as in chimpanzees, visual preferences of agile gibbons are not genetically programmed but develop through social experience during infancy.     

Phenotypic Variation in Infants,Not Adults,Reflects Genotypic Variation among Chimpanzees and Bonobos

Studies comparing phenotypic variation with neutral genetic variation in modern humans have shown that genetic drift is a main factor of evolutionary diversification among populations. The genetic population history of our closest living relatives, the chimpanzees and bonobos, is now equally well documented, but phenotypic variation among these taxa remains relatively unexplored, and phenotype-genotype correlations are not yet documented. Also, while the adult phenotype is typically used as a reference, it remains to be investigated how phenotype-genotye correlations change during development. Here we address these questions by analyzing phenotypic evolutionary and developmental diversification in the species and subspecies of the genus Pan. Our analyses focus on the morphology of the femoral diaphysis, which represents a functionally constrained element of the locomotor system. Results show that during infancy phenotypic distances between taxa are largely congruent with non-coding (neutral) genotypic distances. Later during ontogeny, however, phenotypic distances deviate from genotypic distances, mainly as an effect of heterochronic shifts between taxon-specific developmental programs. Early phenotypic differences between Pan taxa are thus likely brought about by genetic drift while late differences reflect taxon-specific adaptations.     

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.     

Chimpanzee sociability is associated with vasopressin (Avpr1a) but not oxytocin receptor gene (OXTR) variation

The importance of genes in regulating phenotypic variation of personality traits in humans and animals is becoming increasingly apparent in recent studies. Here we focus on variation in the vasopressin receptor gene 1a (Avpr1a) and oxytocin receptor gene (OXTR) and their effects on social personality traits in chimpanzees. We combine newly available genetic data on Avpr1a and OXTR allelic variation of 62 captive chimpanzees with individual variation in personality, based on behavioral assessments. Our study provides support for the positive association of the Avpr1a promoter region, in particular the presence of DupB, and sociability in chimpanzees. This complements findings of previous studies on adolescent chimpanzees and studies that assessed personality using questionnaire data. In contrast, no significant associations were found for the single nucleotide polymorphism (SNP) ss1388116472 of the OXTR and any of the personality components. Most importantly, our study provides additional evidence for the regulatory function of the 5′ promoter region of Avpr1a on social behavior and its evolutionary stable effect across species, including rodents, chimpanzees and humans. Although it is generally accepted that complex social behavior is regulated by a combination of genes, the environment and their interaction, our findings highlight the importance of candidate genes with large effects on behavioral variation.     

Developmental patterns of chimpanzee cerebral tissues provide important clues for understanding the remarkable enlargement of the human brain

Developmental prolongation is thought to contribute to the remarkable brain enlargement observed in modern humans (Homo sapiens). However, the developmental trajectories of cerebral tissues have not been explored in chimpanzees (Pan troglodytes), even though they are our closest living relatives. To address this lack of information, the development of cerebral tissues was tracked in growing chimpanzees during infancy and the juvenile stage, using three-dimensional magnetic resonance imaging and compared with that of humans and rhesus macaques (Macaca mulatta). Overall, cerebral development in chimpanzees demonstrated less maturity and a more protracted course during prepuberty, as observed in humans but not in macaques. However, the rapid increase in cerebral total volume and proportional dynamic change in the cerebral tissue in humans during early infancy, when white matter volume increases dramatically, did not occur in chimpanzees. A dynamic reorganization of cerebral tissues of the brain during early infancy, driven mainly by enhancement of neuronal connectivity, is likely to have emerged in the human lineage after the split between humans and chimpanzees and to have promoted the increase in brain volume in humans. Our findings may lead to powerful insights into the ontogenetic mechanism underlying human brain enlargement.     

Social Attention in the Two Species of Pan: Bonobos Make More Eye Contact than Chimpanzees

Humans’ two closest primate living relatives, bonobos and chimpanzees, differ behaviorally, cognitively, and emotionally in several ways despite their general similarities. While bonobos show more affiliative behaviors towards conspecifics, chimpanzees display more overt and severe aggression against conspecifics. From a cognitive standpoint, bonobos perform better in social coordination, gaze-following and food-related cooperation, while chimpanzees excel in tasks requiring extractive foraging skills. We hypothesized that attention and motivation play an important role in shaping the species differences in behavior, cognition, and emotion. Thus, we predicted that bonobos would pay more attention to the other individuals’ face and eyes, as those are related to social affiliation and social coordination, while chimpanzees would pay more attention to the action target objects, as they are related to foraging. Using eye-tracking we examined the bonobos’ and chimpanzees’ spontaneous scanning of pictures that included eyes, mouth, face, genitals, and action target objects of conspecifics. Although bonobos and chimpanzees viewed those elements overall similarly, bonobos viewed the face and eyes longer than chimpanzees, whereas chimpanzees viewed the other elements, the mouth, action target objects and genitals, longer than bonobos. In a discriminant analysis, the individual variation in viewing patterns robustly predicted the species of individuals, thus clearly demonstrating species-specific viewing patterns. We suggest that such attentional and motivational differences between bonobos and chimpanzees could have partly contributed to shaping the species-specific behaviors, cognition, and emotion of these species, even in a relatively short period of evolutionary time.     

Brain Size Growth and Life History in Human Evolution

Increases in endocranial volume (a measure of brain size) play a major role in human evolution. Despite the importance of brain size increase, the developmental bases of human brain size evolution remain poorly characterized. Comparative analyses of endocranial volume size growth illustrate that distinctions between humans and other primates are consequences of differences in rates of brain size growth, with little evidence for differences in growth duration. Evaluation of available juvenile fossils shows that earliest hominins do not differ perceptibly from chimpanzees (Pan). However, rapid and human-like early brain growth apparently characterized Homo erectus at about 1?Ma before present. Neandertals show patterns of brain growth consistent with modern humans during infancy, but reach larger sizes than modern humans as a result of differences in later growth. Growth analyses reveal commonalities in patterns of early brain size growth during the last million years human evolution, despite major increases in adult size. This result implies consistency across hominins in terms of maternal metabolic costs of infancy. Continued size growth past infancy in Neandertals and modern humans, when compared to earlier hominins, may have cognitive implications. Differences between Neandertals and modern humans are implied, but difficult to define with certainty.     

AVPR1A variation is linked to gray matter covariation in the social brain network of chimpanzees

The vasopressin system has been implicated in the regulation of social behavior and cognition in humans, nonhuman primates and other social mammals. In chimpanzees, polymorphisms in the vasopressin V1a receptor gene (AVPR1A) have been associated with social dimensions of personality, as well as to responses to sociocommunicative cues and mirror self‐recognition. Despite evidence of this association with social cognition and behavior, there is little research on the neuroanatomical correlates of AVPR1A variation. In the current study, we tested the association between AVPR1A polymorphisms in the RS3 promotor region and gray matter covariation in chimpanzees using magnetic resonance imaging and source‐based morphometry. The analysis identified 13 independent brain components, three of which differed significantly in covariation between the two AVPR1A genotypes (DupB?/? and DupB+/?; P < .05). DupB+/? chimpanzees showed greater covariation in gray matter in the premotor and prefrontal cortex, basal forebrain, lunate and cingulate cortex, and lesser gray matter covariation in the superior temporal sulcus and postcentral sulcus. Some of these regions were previously found to differ in vasopressin and oxytocin neural fibers between nonhuman primates, and in AVPR1A gene expression in humans with different RS3 alleles. This is the first report of an association between AVPR1A and gray matter covariation in nonhuman primates, and specifically links an AVPR1A polymorphism to structural variation in the social brain network. These results further affirm the value of chimpanzees as a model species for investigating the relationship between genetic variation, brain structure and social cognition with relevance to psychiatric disorders, including autism.     

Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees

Research on age-related changes in morphology, social behavior, and cognition suggests that the development of bonobos (Pan paniscus) is delayed in comparison to chimpanzees (Pan troglodytes). However, there is also evidence for earlier reproductive maturation in bonobos. Since developmental changes such as reproductive maturation are induced by a number of endocrine processes, changes in hormone levels are indicators of different developmental stages. Age-related changes in testosterone excretion are an indirect marker for the onset of puberty in human and non-human primates. In this study we investigated patterns of urinary testosterone levels in male and female bonobos and chimpanzees to determine the onset of puberty. In contrast to other studies, we found that both species experience age-related changes in urinary testosterone levels. Older individuals of both sexes had significantly higher urinary testosterone levels than younger individuals, indicating that bonobos and chimpanzees experience juvenile pause. The males of both species showed a similar pattern of age-related changes in urinary testosterone levels, with a sharp increase in levels around the age of eight years. This suggests that species-differences in aggression and male mate competition evolved independently of developmental changes in testosterone levels. Females showed a similar pattern of age-related urinary testosterone increase. However, in female bonobos the onset was about three years earlier than in female chimpanzees. The earlier rise of urinary testosterone levels in female bonobos is in line with reports of their younger age of dispersal, and suggests that female bonobos experience puberty at a younger age than female chimpanzees.     

Is culture a golden barrier between human and chimpanzee?

Culture pervades much of human existence. Its significance to human social interaction and cognitive development has convinced some researchers that the phenomenon and its underlying mechanisms represent a defining criterion for humankind. However, care should be taken not to make hasty conclusions in light of the growing number of observations on the cultural abilities of different species, ranging from chimpanzees and orangutans to whales and dolphins. The present review concentrates on wild chimpanzees and shows that they all possess an extensive cultural repertoire. In the light of what we know from humans, I evaluate the importance of social learning leading to acquisition of cultural traits, as well as of collective meaning of communicative traits. Taking into account cross‐cultural variations in humans, I argue that the cultural abilities we observe in wild chimpanzees present a broad level of similarity between the two species.     

Primate Innovation: Sex,Age and Social Rank Differences

Analysis of an exhaustive survey of primate behavior collated from the published literature revealed significant variation in rates of innovation among individuals of different sex, age and social rank. We searched approximately 1,000 articles in four primatology journals, together with other relevant databases, for examples of innovation. The reported incidence of innovation is higher in males and adults, and lower in females and nonadults, than would be expected by chance given the estimated relative proportions of these groups. Amongst chimpanzees, the only species for which there are sufficient data to consider alone, there is a similar sex difference in the propensity to innovate, but no effect of age. Chimpanzees of low social rank are reported as innovators more frequently than high-ranking chimpanzees are. Male chimpanzees innovate more often than females in sexual, courtship, mating and display contexts; that is, in contexts likely to increase access to mates. The largest number of recorded observations are in the foraging context, wherein contrary to expectations, there is no evidence for female chimpanzees exhibiting more innovation than males. The study is the first extensive investigation of behavioral innovation in primates and provides evidence that much individual variation in the propensity to innovate can be explained in terms of sex, age, and social rank.     

Cultural panthropology

Culture, in the most basic sense of “tradition,” has been shown to exist in many species. There is more to the phenomenon of culture in humans, however, than the mere existence of traditions. Thus, rather than expecting that culture can be assigned to living or ancestral species in an all‐or‐none fashion, reconstruction of the evolution of this uniquely complex phenomenon is likely to depend on successfully teasing apart its components, which may have evolved in a somewhat mosaic fashion. In this paper, we dissect ten different aspects of human culture and offer evidence that most of them are manifested in chimpanzees, even if in limited ways, permitting inferences about the cultural profile of our common ancestor. The aspects of culture examined include large‐scale patterns of behavioral variation across populations, the mechanisms available for social transmission, and cultural contents. The contrasts thus drawn for humans and chimpanzees offer a framework for cultural comparisons between other taxa from the past and present.