Jeroen Stevens

Aggression and dominance in matched groups of subadult Icelandic horses (Equus caballus)

We studied sex differences in the nature of aggression and dominance behaviour in two newly formed groups of 1-year-old Icelandic horses. One herd contained nine geldings, the other nine mares. The groups were matched with regard to dominance-determining traits such as age, weaning age, composition of native herd, social experience, genetic origin, body condition and maternal dominance status. High-ranking individuals of both sexes were more aggressive, high-ranking males were older, and high-ranking females had a better body condition. Frequencies of aggressions were similar in both groups. The mares reacted significantly more by showing submission upon an aggression rather than by not responding or by escalating the aggression. For the geldings, this difference was not observed due to a lower tendency to submit. A linear dominance hierarchy was found in both groups. David’s scores provided additional information regarding cardinal rank distances and were used to calculate steepness of hierarchies. The female hierarchy was somewhat steeper compared to the male hierarchy, suggesting somewhat lower despotism among males. This was mainly a consequence of the lower unidirectionality in male submission. Male contests occurred predominantly between dyads at top and mid positions, suggesting a low degree of acceptance of the hierarchy.

The influence of the steepness of dominance hierarchies on reciprocity and interchange in captive groups of bonobos (**Pan paniscus**)

Summary Biological market models explain variability in reciprocity and interchange between groups. In groups with a shallow dominance gradient, grooming will be mostly exchanged for itself (i.e. exchange will occur). In groups with steep dominance hierarchies, interchange is expected: individuals will groom higher ranking individuals to get access to limited resources or commodities such as support in conflicts, and grooming will be traded for these commodities. We examine patterns of reciprocity in grooming and support, and of interchange of grooming for support or for tolerance in six captive groups of bonobos. We test whether differences between groups in patterns of reciprocity and interchange can be attributed to differences in a measure of steepness of dominance hierarchies, which is based on dyadic agonistic interactions. We found that grooming was reciprocal in some, but not all groups. Support was highly reciprocal, but this was a side effect of dominance in most groups. Interchange between grooming and support was observed in some groups. Corroborating earlier findings, this was a side effect of individuals preferring high ranking individuals as grooming and support partners, possibly because these high-ranking individuals provide more efficient support in conflicts. There was no evidence for interchange of grooming for tolerance. Variability in grooming reciprocity was explained by differences in steepness of dominance hierarchies, as predicted by the biological market models. In groups with a shallow dominance hierarchy, grooming was more reciprocal. This was not true for reciprocity in

Sex Differences in the Steepness of Dominance Hierarchies in Captive Bonobo Groups

Bonobos have a reputation as a female-dominated and egalitarian species. We examined the 2 aspects of dominance in 6 captive bonobo groups. Females do not consistently evoke submission from all males in all contexts. Though females occupy the highest-ranking positions in the dominance hierarchy, there are in each group males that obtain rather high ranks and are able to dominate ≥1 female. Thus female dominance is not complete and hierarchies can be better described as nonexclusive female dominance. We studied egalitarianism by measuring linearity and steepness of dominance hierarchies. The hierarchies of all groups are highly linear. Hierarchies among males are steeper than among females. On average, male bonobos are more despotic than females, but females too can have despotic relations, both with other females and with males. Hence one can call bonobos in captivity semidespotic rather than egalitarian.

Social structures in Pan paniscus : testing the female bonding hypothesis

Based on previous research in captivity, bonobos, Pan paniscus, have been called a female-bonded species. However, genetic and behavioural data indicate that wild females migrate. Bonding between these unrelated females would then be in contradiction with socio-ecological models. It has been argued that female bonding has been overemphasized in captive bonobos. We examine patterns of proximity, grooming and support behaviour in six well established captive groups of bonobos. We find that female bonding was not a typical characteristic of all captive bonobo groups. In only two groups there was a trend for females to prefer proximity with other females over association with males. We found no evidence that following or grooming between females was more frequent than between males and unrelated females or between males. Only in coalitions, females supported each other more than male–female or male–male dyads. We also investigated five mother–son pairs. Grooming was more frequent among mothers and sons than in any other dyad, but sons did not groom their mothers more than males groomed unrelated females. Mothers groomed their sons, or provided more support to them than females groomed or supported unrelated males. Thus, while bonds between females were clearly present, intersexual relations between males and either unrelated females or their mothers are of more, or equal importance.

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.

Adrenarche in bonobos (Pan paniscus): evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels

Adrenarche is characterized by the onset of adrenal secretions of increasing amounts of dehydroepiandrosterone-sulfate (DHEA-S). While the function of adrenarche remains a matter of speculation, evidence suggests that the morphological and physiological changes related to it are restricted to humans and closely related primates. Within the primate order, adrenarche has been described only in humans and chimpanzees, but bonobos, the sister species of chimpanzees, have not yet been studied regarding the early ontogenetic changes such as adrenarche. While bonobos and chimpanzees share many morphological and behavioral characteristics, they differ in a number of behavioral traits, and there is a growing interest in terms of the physiological differences that can be linked to species-specific patterns of social behavior. In this study, we measured urinary DHEA-S levels to determine whether bonobos experience physiological changes that are indicative of adrenarche. We measured DHEA-S in urine using ELISA and analyzed its levels in the samples from 53 bonobos aged 1-18 years. Our results show that bonobos experience an increase in DHEA-S levels after 5 years of age, which is comparable with the patterns observed in humans and chimpanzees. This indicates that bonobos do undergo adrenarche and that the timing of onset is similar to that of the two Pan species. The extraction procedures described in this report demonstrate the use of urine for monitoring ontogenetic changes in DHEA-S excretion. If applicable to other species, the technique would facilitate more research on the evolutionary origin of adrenarche and other developmental processes.

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.

Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus)

In the recent past, application of DNA genotyping techniques has enabled researchers to more accurately test relationships between dominance rank (DR), mating success (MS) and reproductive success (RS). Paternity studies often reveal that reproductive outcome does not always correlate with male DR and/or MS and thus open room for discussion and interpretation of alternative reproductive tactics of both sexes. In this study, we analysed male DR, MS and RS in a group of bonobos at Twycross Zoo (UK). Genetic relationships were determined using 8 tetrameric microsatellite loci. Despite clear and asymmetric dominance relationships, analysed using normalised David’s scores based on a dyadic index of dominance among the group’s 3 mature males, we found that the most dominant male did not sire the most offspring. In fact, both infants conceived during the observation period were found to be sired by the lower-ranking males. Although the alpha male had almost exclusive mating access to one of the females during the time she was showing a maximal anogenital swelling, her infant was sired by the lowest-ranking male who mostly mated with her when outside the maximal swelling period. This result suggests that either sperm competition operates and/or ovulation is decoupled from the phase of maximal anogenital swelling which could allow greater female choice.

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.