Nicky Staes

Oxytocin and Vasopressin Receptor Gene Variation as a Proximate Base for Inter- and Intraspecific Behavioral Differences in Bonobos and Chimpanzees

Recent literature has revealed the importance of variation in neuropeptide receptor gene sequences in the regulation of behavioral phenotypic variation. Here we focus on polymorphisms in the oxytocin receptor gene (OXTR) and vasopressin receptor gene 1a (Avpr1a) in chimpanzees and bonobos. In humans, a single nucleotide polymorphism (SNP) in the third intron of OXTR (rs53576 SNP (A/G)) is linked with social behavior, with the risk allele (A) carriers showing reduced levels of empathy and prosociality. Bonobos and chimpanzees differ in these same traits, therefore we hypothesized that these differences might be reflected in variation at the rs53576 position. We sequenced a 320 bp region surrounding rs53576 but found no indications of this SNP in the genus Pan. However, we identified previously unreported SNP variation in the chimpanzee OXTR sequence that differs from both humans and bonobos. Humans and bonobos have previously been shown to have a more similar 5′ promoter region of Avpr1a when compared to chimpanzees, who are polymorphic for the deletion of ∼360 bp in this region (+/− DupB) which includes a microsatellite (RS3). RS3 has been linked with variation in levels of social bonding, potentially explaining part of the interspecies behavioral differences found in bonobos, chimpanzees and humans. To date, results for bonobos have been based on small sample sizes. Our results confirmed that there is no DupB deletion in bonobos with a sample size comprising approximately 90% of the captive founder population, whereas in chimpanzees the deletion of DupB had the highest frequency. Because of the higher frequency of DupB alleles in our bonobo population, we suggest that the presence of this microsatellite may partly reflect documented differences in levels of sociability found in bonobos and chimpanzees.

Personality in Bonobos

To better understand human and chimpanzee personality evolution, we obtained trait ratings of personality for 154 captive bonobos (~80% of the U.S. and European population). We found factors that we labeled Assertiveness, Conscientiousness, Openness, Agreeableness, Attentiveness, and Extraversion. The interrater reliabilities and test-retest reliabilities for these factors were comparable to those found in humans and other species. Using orthogonal targeted Procrustes rotations, we compared the bonobo dimensions with those of three samples of captive chimpanzees. Overall congruence coefficients indicated a fair degree of similarity; at the factor level, there was good evidence for Assertiveness, Conscientiousness, Openness, and Agreeableness in the chimpanzee samples; evidence for Attentiveness and Extraversion was poor. These findings suggest that, as expected given their close phylogenetic relationship, bonobo personality structure resembles chimpanzee personality structure in some respects. However, divergent evolution, perhaps as a result of socioecological differences between bonobos and chimpanzees, also appears to have shaped personality structure in these species.

Bonobo personality traits are heritable and associated with vasopressin receptor gene 1a variation

Despite being closely related, bonobos and chimpanzees show remarkable behavioral differences, the proximate origins of which remain unknown. This study examined the link between behavioral variation and variation in the vasopressin 1a receptor gene (Avpr1a) in bonobos. Chimpanzees are polymorphic for a ~360 bp deletion (DupB), which includes a microsatellite (RS3) in the 5′ promoter region of Avpr1a. In chimpanzees, the DupB deletion has been linked to lower sociability, lower social sensitivity, and higher anxiety. Chimpanzees and bonobos differ on these traits, leading some to believe that the absence of the DupB deletion in bonobos may be partly responsible for these differences, and to the prediction that similar associations between Avpr1a genotypes and personality traits should be present in bonobos. We identified bonobo personality dimensions using behavioral measures (SociabilityB, BoldnessB, OpennessB, ActivityB) and trait ratings (AssertivenessR, ConscientiousnessR, OpennessR, AgreeablenessR, AttentivenessR, ExtraversionR). In the present study we found that all 10 dimensions have nonzero heritabilities, indicating there is a genetic basis to personality, and that bonobos homozygous for shorter RS3 alleles were lower in AttentivenessR and higher in OpennessB. These results suggest that variations in Avpr1a genotypes explain both within and between species differences in personality traits of bonobos and chimpanzees.

Relationship quality in captive bonobo groups

We use Principal Component Analyses (PCA) to describe components of social relationship quality in bonobos. We find a three component structure, with the first two components, labelled Value and Compatibility, closely matching the theoretical constructs as well as components reported for chimpanzees and other primates. The third component differed but was abandoned based on Parallel Analysis. Among bonobos, female–female dyads have higher Value and Compatibility. Relationships between males are characterised by low Value and Compatibility. Dyads that had been housed together for a longer time and maternally related ones also have more valuable relationships, while individuals close in rank have low compatibility. The results confirm the strong bonds among female bonobos, but for the first time can describe how they differ qualitatively from close bonds reported for captive chimpanzee females. We suggest future studies should also include Parallel Analysis to more accurately describe the number of components in relationship quality.