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

Abstract

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.

A human model for primate personality

“…Results consistent with these findings have been found in studies that use behavioural measures, including one of semi-free-ranging female rhesus macaques [67] and one of zoo-housed bonobos [75].…”

“…Studies using these statistical methods have found a moderate proportion of the variation in rating-based personality dimensions of chimpanzees [72,73], orangutans [74] and bonobos [75] to be attributable to additive genetic effects. Results consistent with these findings have been found in studies that use behavioural measures, including one of semi-free-ranging female rhesus macaques [67] and one of zoo-housed bonobos [75].…”

Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior

“…Staes et al (2015) also looked at captive chimpanzee personality, but used observed rates of specific behaviors to assess personality rather than questionnaire ratings, and reported that the long allele was associated with total time spent giving and receiving grooming. Staes et al (2016) reported a study of the same polymorphism in captive bonobos rather than chimpanzees, using both observer questionnaires and behavioral rate observations, and found the long allele associated with higher “attentiveness” and lower “openness.” To our knowledge only Staes et al (2015) has examined OXTR in NHPs social behavior, which reported no effect of an intronic SNV.…”

Studying primate personality in zoos: implications for the management, welfare and conservation of great apes

“…Research on zoohoused Chimpanzees (Weiss et al, 2000;Wilson, V. A. D., et al, 2017), orangutans Pongo spp (Adams et al, 2012) and Bonobos Pan paniscus (Staes et al, 2016) has indicated that personality variation appears to be partly related to genetic differences between individuals and partly related to the influences of environmental effects that operate at the within-zoo or within-family level. At the time of writing, no comparable study has been conducted on gorillas Gorilla spp.…”

“…Reif & Lesch, 2003). Studies of Chimpanzees living at Yerkes National Primate Research Center (Atlanta, GA, USA) (Hopkins et al, 2012;Latzman et al, 2015), and those living mostly in zoos, research centres and a sanctuary in Japan, amounting to 129 Chimpanzees including 19 that lived at a sanctuary in Guinea (Wilson, V. A. D., et al, 2017), found evidence that versions of a gene for receptors for the hormone vasopressin are associated with the personality dimension Conscientiousness, which describes how tame and predictable individuals are [see Staes et al (2016) for a similar finding in Bonobos]. However, the effects of single genes are very small, typically accounting for <1% of trait variation.…”