30 results on '"Staes N"'
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2. Qualitative Behavioural Assessment of bonobo emotional expressivity across observer groups and zoo housing environments.
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Laméris DW, Salas M, Eens M, Gillespie L, Staes N, Torfs JR, Verspeek J, Vervaecke H, Ward SJ, and Stevens JM
- Abstract
Human evaluation of animal emotional expressivity can inform animal welfare. Qualitative Behavioural Assessment (QBA) has been applied to domesticated and some non-domesticated animals, but its use in primates is limited despite their emotional expressivity. We aimed to develop and apply a QBA for bonobos ( Pan paniscus ) through two consecutive studies. We applied Free Choice Profiling (FCP) and the Fixed List methodology, respectively, in Study 1 and 2, and invited students and bonobo experts to rate video clips of zoo-living bonobos of different sexes and age classes, and before and after moving to a new enclosure. In Study 1, students described dimension 1 as ranging from 'quiet/calm' to 'angry/active' and dimension 2 from 'sad/anxious' to 'happy/loving'. Experts described dimension 1 ranging from 'quiet/relaxed' to 'nervous/alert' and dimension 2 from 'nervous/bored' to 'playful/happy'. Using a fixed list of descriptors, informed by findings from Study 1, students in Study 2 described dimension 1 as ranging from 'quiet/calm' to 'agitated/frustrated', and dimension 2 from 'sad/stressed' to 'happy/positively engaged'. Experts described dimension 1 as ranging from 'quiet/calm' to 'active/excited', and dimension 2 from 'sad/bored' to 'happy/positively engaged'. Students scored adults as more 'calm/quiet' and experts scored subadults as more 'happy/positively engaged'. Additionally, experts in Study 2 rated bonobos as more 'active/excited' in their new enclosure. Reliability was moderate to good for the dimensions. Additionally, animal-directed empathy of observers influenced QBA scores. This is the first time, FCP has been successfully used as a method to study primate emotional expressivity. Our findings show the promise of employing QBA in primate studies and in industry, with validation of additional metrics to enable its use for welfare-monitoring purposes., Competing Interests: None., (© The Author(s) 2024.)
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- 2024
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3. Group-specific expressions of co-feeding tolerance in bonobos and chimpanzees preclude dichotomous species generalizations.
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van Leeuwen EJC, Staes N, Brooker JS, Kordon S, Nolte S, Clay Z, Eens M, and Stevens JMG
- Abstract
Bonobos are typically portrayed as more socially tolerant than chimpanzees, yet the current evidence supporting such a species-level categorization is equivocal. Here, we used validated group-level co-feeding assays to systematically test expressions of social tolerance in sixteen groups of zoo- and sanctuary-housed bonobos and chimpanzees. We found that co-feeding tolerance substantially overlaps between the species, thus precluding categorical inference at the species level. Instead, marked differences were observed between groups, with some bonobo communities exhibiting higher social tolerance than chimpanzee communities, and vice versa. Moreover, considerable intergroup variation was found within species living in the same environment, which attests to Pan 's behavioral flexibility. Lastly, chimpanzees showed more tolerance in male-skewed communities, whereas bonobos responded less pronounced to sex-ratio variation. We conclude that the pervasive dichotomy between the tolerant bonobo and the belligerent chimpanzee requires quantitative nuance, and that accurate phylogenetic tracing of (human) social behavior warrants estimations of intraspecific group variation., Competing Interests: The authors declare no competing interests., (© 2023 The Authors.)
- Published
- 2023
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4. Visually assessed body condition shows high heritability in a pedigreed great ape population.
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Torfs JRR, Eens M, Laméris DW, Stevens JMG, Verspeek J, Guery JP, and Staes N
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- Animals, Reproducibility of Results, Pan troglodytes, Body Weight genetics, Pan paniscus genetics, Hominidae
- Abstract
Body condition, a measure for relative fat mass, is associated with primate health, fitness, and overall welfare. Body condition is often influenced by dietary factors, age, and/or sex, but several body condition measures (body weight, weight-to-height ratios, and so on) also show high heritability across primate species, indicating a role of genetic effects. Although different measures for body condition exist, many require direct handling of animals, which is invasive, time-consuming, and expensive, making them impractical in wild and captive settings. Therefore, noninvasive visual body condition score (BCS) systems were developed for various animal species, including macaques and chimpanzees, to visually assess relative fat mass. Here we evaluate the utility of a visual BCS system in bonobos by assessing (1) inter-rater reliability, (2) links with body mass, a traditional hands-on measure of condition, and (3) the factors driving individual variation in BCS. We adapted the chimpanzee BCS system to rate 76 bonobos in 11 European zoos (92% of the adult population). Inter-rater reliability was high (s* = 0.948), BCSs were positively associated with body mass (β = 0.075) and not predicted by diet, sex, or age, nor were they associated with a higher abundance of obesity-related diseases. Instead, BCSs showed high levels of heritability (h
2 = 0.637), indicating that a majority of body condition variation in bonobos is attributable to genetic similarity of the individuals. This is in line with reported h2 -values for traditional body condition measures in primates and provides support for the reliability of visual BCS systems in great apes. The results of this study emphasize an often unanticipated role of genetics in determining primate body fat and health that has implications for the management of captive primates. Application of this tool in wild populations would aid to unravel environmental from genetic drivers of body condition variation in primates., (© 2023 Wiley Periodicals LLC.)- Published
- 2023
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5. Multi-group analysis of grooming network position in a highly social primate.
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Torfs JRR, Stevens JMG, Verspeek J, Laméris DW, Guéry JP, Eens M, and Staes N
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- Animals, Female, Male, Grooming, Sex Ratio, Social Behavior, Pan paniscus
- Abstract
Individual variation in complex social behavioral traits, like primate grooming, can be influenced by the characteristics of the individual and those of its social group. To better grasp this complexity, social network analysis can be used to quantify direct and indirect grooming relationships. However, multi-group social network studies remain rare, despite their importance to disentangle individual from group-level trait effects on grooming strategies. We applied social network analysis to grooming data of 22 groups of zoo-housed bonobos and investigated the impact of three individual (sex, age, and rearing-history) and two group-level traits (group size and sex ratio) on five social network measures (out-strength, in-strength, disparity, affinity, and eigenvector centrality). Our results showed age-effects on all investigated measures: for females, all measures except for affinity showed quadratic relationships with age, while in males, the effects of age were more variable depending on the network measure. Bonobos with atypical rearing histories showed lower out-strength and eigenvector centrality, while in-strength was only impacted by rearing history in males. Group size showed a negative association with disparity and eigenvector centrality, while sex ratio did not influence any of the investigated measures. Standardization for group size did not impact the effects of sex and age, indicating the robustness of these findings. Our study provides comprehensive insights into the complexity of grooming behavior in zoo-housed bonobos, and underlines the importance of multi-group analyses for the generalizability of social network analysis results for species as a whole., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Torfs et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
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- 2023
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6. Vasopressin, and not oxytocin, receptor gene methylation is associated with individual differences in receptive joint attention in chimpanzees (Pan troglodytes).
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Hopkins WD, Staes N, Guevara EE, Mulholland MM, Sherwood CC, and Bradley BJ
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- Child, Animals, Humans, Pan troglodytes genetics, Social Behavior, Individuality, Methylation, Receptors, Vasopressin genetics, Vasopressins, Attention, Oxytocin, Autism Spectrum Disorder genetics
- Abstract
Joint attention (JA) is an important milestone in human infant development and is predictive of the onset of language later in life. Clinically, it has been reported that children at risk for or with a diagnosis of autism spectrum disorder (ASD) perform more poorly on measures of JA compared to neurotypical controls. JA is not unique to humans but has also been reported in great apes and to a lesser extent in more distantly related monkeys. Further, individual differences in JA among chimpanzees are associated with polymorphisms in the vasopressin and oxytocin genes, AVPR1A and OXTR. Here, we tested whether individual variation in DNA methylation of OXTR and AVPR1A were associated with performance on JA tasks in chimpanzees. We found that individual differences in JA performance was associated with AVPR1A methylation, but not OXTR methylation in the chimpanzees. The collective results provide further evidence of the role of AVPR1A in JA abilities in chimpanzees. The results further suggest that methylation values for AVPR1A may be useful biomarkers for identifying individuals at risk for ASD or related neurodevelopmental disorders associated with impairments in JA abilities., (© 2023 International Society for Autism Research and Wiley Periodicals LLC.)
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- 2023
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7. Genetic determinants of individual variation in the superior temporal sulcus of chimpanzees (Pan troglodytes).
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Hopkins WD, Coulon O, Meguerditchian A, Staes N, Sherwood CC, Schapiro SJ, Mangin JF, and Bradley B
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- Animals, Humans, Genotype, Alleles, Temporal Lobe, Pan troglodytes genetics, Polymorphism, Single Nucleotide
- Abstract
The superior temporal sulcus (STS) is a conserved fold that divides the middle and superior temporal gyri. In humans, there is considerable variation in the shape, folding pattern, lateralization, and depth of the STS that have been reported to be associated with social cognition and linguistic functions. We examined the role that genetic factors play on individual variation in STS morphology in chimpanzees. The surface area and depth of the STS were quantified in sample of 292 captive chimpanzees comprised of two genetically isolated population of individuals. The chimpanzees had been previously genotyped for AVPR1A and KIAA0319, two genes that play a role in social cognition and communication in humans. Single nucleotide polymorphisms in the KIAA0319 and AVPR1A genes were associated with average depth as well as asymmetries in the STS. By contrast, we found no significant effects of these KIA0319 and AVPR1A polymorphism on surface area and depth measures for the central sulcus. The overall findings indicate that genetic factors account for a small to moderate amount of variation in STS morphology in chimpanzees. These findings are discussed in the context of the role of the STS in social cognition and language in humans and their potential evolutionary origins., (© The Author(s) 2022. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)
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- 2023
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8. Chimpanzee Extraversion scores vary with epigenetic modification of dopamine receptor gene D2 ( DRD2 ) and early rearing conditions.
- Author
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Staes N, White CM, Guevara EE, Eens M, Hopkins WD, Schapiro SJ, Stevens JMG, Sherwood CC, and Bradley BJ
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- Animals, DNA Methylation, Personality genetics, Epigenesis, Genetic, Extraversion, Psychological, Pan troglodytes genetics, Receptors, Dopamine D2 genetics
- Abstract
Chimpanzees have consistent individual differences in behaviour, also referred to as personality. Similar to human personality structure, five dimensions are commonly found in chimpanzee studies that show evidence for convergent and predictive validity (Dominance, Openness, Extraversion, Agreeableness, and Reactivity/Undependability). These dimensions are to some extent heritable, indicating a genetic component that explains part of the variation in personality scores, but are also influenced by environmental factors, such as the early social rearing background of the individuals. In this study, we investigated the role of epigenetic modification of the dopamine receptor D2 gene ( DRD2 ) as a potential mechanism underlying personality variation in 51 captive chimpanzees. We used previously collected personality trait rating data and determined levels of DRD2 CpG methylation in peripheral blood samples for these same individuals. Results showed that DRD2 methylation is most strongly associated with Extraversion, and that varying methylation levels at specific DRD2 sites are associated with changes in Extraversion in nursery-reared, but not mother-reared, individuals. These results highlight the role of dopaminergic signalling in chimpanzee personality, and indicate that environmental factors, such as social experiences early in life, can have long-lasting behavioural effects, potentially through modification of the epigenome. These findings add to the growing evidence demonstrating the importance of the experience-dependent methylome for the development of complex social traits like personality.
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- 2022
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9. The Role of Serotonergic Gene Methylation in Regulating Anxiety-Related Personality Traits in Chimpanzees.
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Staes N, Guevara EE, Hopkins WD, Schapiro SJ, Eens M, Sherwood CC, and Bradley BJ
- Abstract
While low serotonergic activity is often associated with psychological disorders such as depression, anxiety, mood, and personality disorders, variations in serotonin also contribute to normal personality differences. In this study, we investigated the role of blood DNA methylation levels at individual CpG sites of two key serotonergic genes (serotonin receptor gene 1A, HTR1A ; serotonin transporter gene, SLC6A4 ) in predicting the personalities of captive chimpanzees. We found associations between methylation at 9/48 CpG sites with four personality dimensions: Dominance, Reactivity/Dependability, Agreeableness, and Openness. Directionality of effects were CpG location-dependent and confirmed a role of serotonergic methylation in reducing anxiety (Dominance) and aggression-related personality (Reactivity/Undependability) while simultaneously promoting prosocial (Agreeableness) and exploratory personalities (Openness). Although early-life adversity has been shown to impact serotonergic methylation patterns in other species, here, atypical early social rearing experiences only had a modest impact on CpG methylation levels in this chimpanzee sample. The precise environmental factors impacting serotonergic methylation in chimpanzees remain to be identified. Nevertheless, our study suggests a role in shaping natural variation in animal personalities. The results of this study offer a basis for future hypothesis-driven testing in additional populations and species to better understand the impact of ecology and evolution on complex behavioral traits.
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- 2022
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10. Evaluating Self-Directed Behaviours and Their Association with Emotional Arousal across Two Cognitive Tasks in Bonobos ( Pan paniscus ).
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Laméris DW, Verspeek J, Salas M, Staes N, Torfs JRR, Eens M, and Stevens JMG
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Self-directed behaviours (SDBs) are widely used as markers of emotional arousal in primates, and are commonly linked to negative arousal, or are used as indicators of stress or poor welfare. However, recent studies suggest that not all SDBs have the same function. Moreover, lateralisation in the production of these behaviours has been suggested to be associated with emotional processing. Hence, a better understanding of the production and the asymmetry of these displacement behaviours is needed in a wider range of species in order to confirm their reliability as indicators of emotional arousal. In the current study, we experimentally evaluated the production and asymmetry of SDBs in zoo-housed bonobos during two cognitive touchscreen tasks. Overall, nose wipes were most commonly observed, followed by gentle self-scratches, and rough self-scratches. The rates of nose wipes and rough self-scratches increased with incorrect responses, suggesting that these behaviours indicate arousal and possibly frustration. Rough self-scratching was additionally more directed towards the left hemispace after incorrect responses. In contrast, gentle self-scratching increased after correct responses in one study, possibly linking it with positive arousal. We also tested if left-handed bonobos showed greater behavioural reactivity towards incorrect responses, but found no evidence to confirm this hypothesis. Our results shed light on potential different mechanisms behind separate SDBs. We therefore provide nuance to the use of SDBs as indicator of emotional arousal in bonobos.
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- 2022
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11. Drivers of Dyadic Cofeeding Tolerance in Pan : A Composite Measure Approach.
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Staes N, Vermeulen K, van Leeuwen EJC, Verspeek J, Torfs JRR, Eens M, and Stevens JMG
- Abstract
This study aimed to construct a composite model of Dyadic Cofeeding Tolerance (DCT) in zoo-housed bonobos and chimpanzees using a validated experimental cofeeding paradigm and to investigate whether components resulting from this model differ between the two species or vary with factors such as sex, age, kinship and social bond strength. Using dimension reduction analysis on five behavioral variables from the experimental paradigm (proximity, aggression, food transfers, negative food behavior, participation), we found a two-factor model: "Tolerant Cofeeding" and "Agonistic Cofeeding". To investigate the role of social bond quality on DCT components alongside species effects, we constructed and validated a novel relationship quality model for bonobos and chimpanzees combined, resulting in two factors: Relationship Value and Incompatibility. Interestingly, bonobos and chimpanzees did not differ in DCT scores, and sex and kinship effects were identical in both species but biased by avoidance of the resource zone by male-male dyads in bonobos. Social bonds impacted DCT similarly in both species, as dyads with high Relationship Value showed more Tolerant Cofeeding, while dyads with higher Relationship Incompatibility showed more Agonistic Cofeeding. We showed that composite DCT models can be constructed that take into account both negative and positive cofeeding behavior. The resulting DCT scores were predicted by sex, kinship and social bonds in a similar fashion in both Pan species, likely reflecting their adaptability to changing socio-ecological environments. This novel operational measure to quantify cofeeding tolerance can now be applied to a wider range of species in captivity and the wild to see how variation in local socio-ecological circumstances influences fitness interdependence and cofeeding tolerance at the dyadic and group levels. This can ultimately lead to a better understanding of how local environments have shaped the evolution of tolerance in humans and other species.
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- 2022
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12. Adult bonobos show no prosociality in both prosocial choice task and group service paradigm.
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Verspeek J, van Leeuwen EJC, Laméris DW, Staes N, and Stevens JMG
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- Animals, Cooperative Behavior, Behavior, Animal, Feeding Behavior, Pan troglodytes, Pan paniscus, Social Behavior
- Abstract
Previous studies reported contrasting conclusions concerning bonobo prosociality, which are likely due to differences in the experimental design, the social dynamics among subjects and characteristics of the subjects themselves. Two hypotheses have been proposed to explain the occurrence of prosociality in animals: the cooperative breeding hypothesis and the self-domestication hypothesis. While the former predicts low levels of prosociality in bonobos because they are non-cooperative breeders, the latter predicts high levels of prosociality because self-domestication has been proposed to select for high levels of tolerance in this species. Here, we presented a group of thirteen bonobos with two platform food-provisioning tasks: the prosocial choice task (PCT) and the group service paradigm (GSP). The latter has so far never been applied to bonobos. To allow for free choice of participation and partner, we implemented both tasks in a group setting. Like in previous PCT studies, bonobos did not choose the prosocial option more often when a group member could benefit vs not benefit. In the GSP, where food provisioning is costly, only subadult bonobos showed a limited amount of food provisioning, which was much lower than what was previously reported for chimpanzees. In both experiments, adult subjects were highly motivated to obtain rewards for themselves, suggesting that bonobos behaved indifferently to the gains of group members. We suggest that previous positive food-provisioning prosociality results in bonobos are mainly driven by the behaviour of subadult subjects. The lack of prosociality in this study corresponds to the hypothesis that proactive food provisioning co-occurs with cooperative breeding and suggests that proactive prosociality might not be part of the self-domestication syndrome in bonobos., Competing Interests: The authors declare that they have no competing interests., (© 2022 Verspeek et al.)
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- 2022
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13. Serotonin transporter (SERT) polymorphisms, personality and problem-solving in urban great tits.
- Author
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Grunst AS, Grunst ML, Staes N, Thys B, Pinxten R, and Eens M
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- Alleles, Animals, Behavior, Animal, Cognition, Ecology, Exons, Female, Genetics, Behavioral, Genotype, Geography, Homozygote, Linkage Disequilibrium, Male, Problem Solving, Reproduction, Passeriformes genetics, Passeriformes physiology, Polymorphism, Single Nucleotide, Serotonin Plasma Membrane Transport Proteins genetics
- Abstract
Understanding underlying genetic variation can elucidate how diversity in behavioral phenotypes evolves and is maintained. Genes in the serotonergic signaling pathway, including the serotonin transporter gene (SERT), are candidates for affecting animal personality, cognition and fitness. In a model species, the great tit (Parus major), we reevaluated previous findings suggesting relationships between SERT polymorphisms, neophobia, exploratory behavior and fitness parameters, and performed a first test of the relationship between single nucleotide polymorphisms (SNPs) in SERT and problem-solving in birds. We found some evidence for associations between SERT SNPs and neophobia, exploratory behavior and laying date. Furthermore, several SNPs were associated with behavioral patterns and success rates during obstacle removal problem-solving tests performed at nest boxes. In females, minor allele homozygotes (AA) for nonsynonymous SNP226 in exon 1 made fewer incorrect attempts and were more likely to problem-solve. In both sexes, there was some evidence that minor allele homozygotes (CC) for SNP84 in exon 9 were more likely to problem-solve. Only one SNP-behavior relationship was statistically significant after correcting for multiple comparisons, but several were associated with substantial effect sizes. Our study provides a foundation for future research on the genetic basis of behavioral and cognitive variation in wild animal populations., (© 2021. The Author(s).)
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- 2021
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14. Respiratory Disease Risk of Zoo-Housed Bonobos Is Associated with Sex and Betweenness Centrality in the Proximity Network.
- Author
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Torfs JRR, Eens M, Laméris DW, and Staes N
- Abstract
Infectious diseases can be considered a threat to animal welfare and are commonly spread through both direct and indirect social interactions with conspecifics. This is especially true for species with complex social lives, like primates. While several studies have investigated the impact of sociality on disease risk in primates, only a handful have focused on respiratory disease, despite it being a major cause of morbidity and mortality in both wild and captive populations and thus an important threat to primate welfare. Therefore, we examined the role of social-network position on the occurrence of respiratory disease symptoms during one winter season in a relatively large group of 20 zoo-housed bonobos with managed fission-fusion dynamics. We found that within the proximity network, symptoms were more likely to occur in individuals with higher betweenness centrality, which are individuals that form bridges between different parts of the network. Symptoms were also more likely to occur in males than in females, independent of their social-network position. Taken together, these results highlight a combined role of close proximity and sex in increased risk of attracting respiratory disease, two factors that can be taken into account for further welfare management of the species.
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- 2021
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15. Gray Matter Variation in the Posterior Superior Temporal Gyrus Is Associated with Polymorphisms in the KIAA0319 Gene in Chimpanzees ( Pan troglodytes ).
- Author
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Hopkins WD, Staes N, Mulholland MM, Schapiro SJ, Rosenstein M, Stimpson C, Bradley BJ, and Sherwood CC
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- Animals, Brain diagnostic imaging, Cerebral Cortex, Magnetic Resonance Imaging, Wernicke Area, Gray Matter diagnostic imaging, Pan troglodytes
- Abstract
Determining the impact that the KIAA0319 gene has on primate brain morphology can provide insight into the evolution of human cognition and language systems. Here, we tested whether polymorphisms in KIAA0319 in chimpanzees account for gray matter volumetric variation in brain regions implicated in language and communication (particularly within the posterior superior temporal gyrus and inferior frontal gyrus). First, we identified the nature and frequencies of single nucleotide variants (SNVs) in KIAA0319 in a sample of unrelated chimpanzees ( Pan troglodytes spp.). Next, we genotyped a subset of SNVs (those important for gene regulation or likely to alter protein structure/function) in a sample of chimpanzees for which in vivo T1-structural magnetic resonance imaging scans had been obtained. We then used source-based morphometry (SBM) to test for whole-brain gray matter covariation differences between chimpanzees with different KIAA0319 alleles. Finally, using histologic sections of 15 postmortem chimpanzee brains, we analyzed microstructural variation related to KIAA0319 polymorphisms in the posterior superior temporal cortex. We found that the SNVs were associated with variation in gray matter within several brain regions, including the posterior superior temporal gyrus (a region associated with language comprehension and production in humans). The microstructure analysis further revealed hemispheric differences in neuropil fraction, indicating that KIAA0319 expression may be involved in regulation of processes related to the formation and maintenance of synapses, dendrites, or axons within regions associated with communication., (Copyright © 2021 Hopkins et al.)
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- 2021
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16. The serotonin transporter gene and female personality variation in a free-living passerine.
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Thys B, Grunst AS, Staes N, Pinxten R, Eens M, and Grunst ML
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- Animals, Female, Gene Frequency, Genetic Association Studies, Polymorphism, Single Nucleotide genetics, Behavior, Animal, Passeriformes genetics, Personality genetics, Serotonin Plasma Membrane Transport Proteins genetics
- Abstract
Quantifying variation in behaviour-related genes provides insight into the evolutionary potential of repeatable among-individual variation in behaviour (i.e. personality). Yet, individuals typically also plastically adjust their behaviour in response to environmental conditions and/or age, thereby complicating the detection of genotype-phenotype associations. Here, using a population of free-living great tits (Parus major), we assessed the association between single nucleotide polymorphisms (SNPs) in the serotonin transporter gene (SERT) and two repeatable behavioural traits, i.e. female-female aggression and female hissing behaviour. For female-female aggression, a trait showing age-related plasticity, we found no evidence for associations with SERT SNPs, even when assessing potential age-dependent effects of SERT genotype on aggression. We also found no strong support for associations between SERT SNPs and hissing behaviour, yet we identified two synonymous polymorphisms (exon 13 SNP66 and exon 12 SNP144) of particular interest, each explaining about 1.3% of the total variation in hissing behaviour. Overall, our results contribute to the general understanding of the biological underpinning of complex behavioural traits and will facilitate further (meta-analytic) research on behaviour-related genes. Moreover, we emphasize that future molecular genetic studies should consider age-dependent genotype-phenotype associations for behavioural trait (co)variation, as this will vastly improve our understanding of the proximate causes and ultimate consequences of personality variation in natural populations.
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- 2021
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17. Time-lag of urinary and salivary cortisol response after a psychological stressor in bonobos (Pan paniscus).
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Verspeek J, Behringer V, Laméris DW, Murtagh R, Salas M, Staes N, Deschner T, and Stevens JMG
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- Animals, Female, Linear Models, Male, Time Factors, Hydrocortisone urine, Pan paniscus psychology, Pan paniscus urine, Saliva chemistry, Stress, Psychological urine
- Abstract
Cortisol is often measured as a marker for stress. Therefore, a profound validation of the time-lag between the stressor and the increase and peak in cortisol levels is needed. No study measured both the urinary and salivary cortisol time-lag after a psychological stressor. In this study, we used a frequent sampling study design to (1) describe the urinary and salivary cortisol pattern during a control day; and (2) characterize the induced excretion pattern of urinary and salivary cortisol after a psychological stressor in six zoo-housed bonobos. Liquid chromatography-tandem mass spectrometry was used to analyze 71 urine and 162 saliva samples collected on a control and a test day. We found that the time-lag between the stressor and the maximal cortisol concentration was similar in urine and saliva (160 min after the stressor). However, salivary cortisol after the stressor did show a faster and steeper increase than urinary cortisol. We also show inter-individual variation in the baseline and stress levels of cortisol, which should be considered in future cortisol studies. Our research highlights the importance of validation studies to confirm relevant sampling windows for cortisol sampling in order to obtain biologically meaningful results.
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- 2021
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18. The Pan social brain: An evolutionary history of neurochemical receptor genes and their potential impact on sociocognitive differences.
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Staes N, Guevara EE, Helsen P, Eens M, and Stevens JMG
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- Animals, Brain metabolism, Pan paniscus metabolism, Pan troglodytes metabolism, Receptors, Dopamine genetics, Receptors, Dopamine metabolism, Receptors, Oxytocin genetics, Receptors, Oxytocin metabolism, Receptors, Serotonin genetics, Receptors, Serotonin metabolism, Receptors, Vasopressin genetics, Receptors, Vasopressin metabolism, Evolution, Molecular, Pan paniscus genetics, Pan troglodytes genetics, Social Cognition
- Abstract
Humans have unique cognitive capacities that, compared with apes, are not only simply expressed as a higher level of general intelligence, but also as a quantitative difference in sociocognitive skills. Humans' closest living relatives, bonobos (Pan paniscus), and chimpanzees (Pan troglodytes), show key between-species differences in social cognition despite their close phylogenetic relatedness, with bonobos arguably showing greater similarities to humans. To better understand the evolution of these traits, we investigate the neurochemical mechanisms underlying sociocognitive skills by focusing on variation in genes encoding proteins with well-documented roles in mammalian social cognition: the receptors for vasopressin (AVPR1A), oxytocin (OXTR), serotonin (HTR1A), and dopamine (DRD2). Although these genes have been well studied in humans, little is known about variation in these genes that may underlie differences in social behavior and cognition in apes. We comparatively analyzed sequence data for 33 bonobos and 57 chimpanzees, together with orthologous sequence data for other apes. In all four genes, we describe genetic variants that alter the amino acid sequence of the respective receptors, raising the possibility that ligand binding or signal transduction may be impacted. Overall, bonobos show 57% more fixed substitutions than chimpanzees compared with the ancestral Pan lineage. Chimpanzees, show 31% more polymorphic coding variation, in line with their larger historical effective population size estimates and current wider distribution. An extensive literature review comparing allelic changes in Pan with known human behavioral variants revealed evidence of homologous evolution in bonobos and humans (OXTR rs4686301(T) and rs237897(A)), while humans and chimpanzees shared OXTR rs2228485(A), DRD2 rs6277(A), and DRD2 rs11214613(A) to the exclusion of bonobos. Our results offer the first in-depth comparison of neurochemical receptor gene variation in Pan and put forward new variants for future behavior-genotype association studies in apes, which can increase our understanding of the evolution of social cognition in modern humans., Competing Interests: Conflicts of interest The authors declare that there are no conflicts of interest to report., (Copyright © 2021 Elsevier Ltd. All rights reserved.)
- Published
- 2021
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19. Age-associated epigenetic change in chimpanzees and humans.
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Guevara EE, Lawler RR, Staes N, White CM, Sherwood CC, Ely JJ, Hopkins WD, and Bradley BJ
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- Animals, Humans, Methylation, Aging, Blood metabolism, Epigenesis, Genetic physiology, Pan troglodytes genetics
- Abstract
Methylation levels have been shown to change with age at sites across the human genome. Change at some of these sites is so consistent across individuals that it can be used as an 'epigenetic clock' to predict an individual's chronological age to within a few years. Here, we examined how the pattern of epigenetic ageing in chimpanzees compares with humans. We profiled genome-wide blood methylation levels by microarray for 113 samples from 83 chimpanzees aged 1-58 years (26 chimpanzees were sampled at multiple ages during their lifespan). Many sites (greater than 65 000) showed significant change in methylation with age and around one-third (32%) of these overlap with sites showing significant age-related change in humans. At over 80% of sites showing age-related change in both species, chimpanzees displayed a significantly faster rate of age-related change in methylation than humans. We also built a chimpanzee-specific epigenetic clock that predicted age in our test dataset with a median absolute deviation from known age of only 2.4 years. However, our chimpanzee clock showed little overlap with previously constructed human clocks. Methylation at CpGs comprising our chimpanzee clock showed moderate heritability. Although the use of a human microarray for profiling chimpanzees biases our results towards regions with shared genomic sequence between the species, nevertheless, our results indicate that there is considerable conservation in epigenetic ageing between chimpanzees and humans, but also substantial divergence in both rate and genomic distribution of ageing-associated sites. This article is part of the theme issue 'Evolution of the primate ageing process'.
- Published
- 2020
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20. Social culture in bonobos.
- Author
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van Leeuwen EJC, Staes N, Verspeek J, Hoppitt WJE, and Stevens JMG
- Subjects
- Animals, Behavior, Animal, Female, Male, Grooming, Pan paniscus psychology, Social Behavior
- Abstract
Van Leeuwen et al. found that two peculiar interactive behaviors (social scratching and groom slapping) transmitted socially through bonobo networks across six European zoos., (Copyright © 2020 Elsevier Inc. All rights reserved.)
- Published
- 2020
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21. Bonobo personality predicts friendship.
- Author
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Verspeek J, Staes N, Leeuwen EJCV, Eens M, and Stevens JMG
- Subjects
- Animals, Female, Male, Behavior, Animal physiology, Pan paniscus physiology, Personality, Social Behavior
- Abstract
In bonobos, strong bonds have been documented between unrelated females and between mothers and their adult sons, which can have important fitness benefits. Often age, sex or kinship similarity have been used to explain social bond strength variation. Recent studies in other species also stress the importance of personality, but this relationship remains to be investigated in bonobos. We used behavioral observations on 39 adult and adolescent bonobos housed in 5 European zoos to study the role of personality similarity in dyadic relationship quality. Dimension reduction analyses on individual and dyadic behavioral scores revealed multidimensional personality (Sociability, Openness, Boldness, Activity) and relationship quality components (value, compatibility). We show that, aside from relatedness and sex combination of the dyad, relationship quality is also associated with personality similarity of both partners. While similarity in Sociability resulted in higher relationship values, lower relationship compatibility was found between bonobos with similar Activity scores. The results of this study expand our understanding of the mechanisms underlying social bond formation in anthropoid apes. In addition, we suggest that future studies in closely related species like chimpanzees should implement identical methods for assessing bond strength to shed further light on the evolution of this phenomenon.
- Published
- 2019
- Full Text
- View/download PDF
22. Evolutionary divergence of neuroanatomical organization and related genes in chimpanzees and bonobos.
- Author
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Staes N, Smaers JB, Kunkle AE, Hopkins WD, Bradley BJ, and Sherwood CC
- Subjects
- Animals, Humans, Pan paniscus, Pan troglodytes, Brain anatomy & histology, Neuroanatomy, Phenotype, Phylogeny, Social Behavior
- Abstract
Given their close genetic relatedness to humans, bonobos (Pan paniscus) and chimpanzees (Pan troglodytes) offer an essential comparative framework for studying the evolution of uniquely human traits. These two species differ markedly in their socio-behavioral repertoires, which is reflected in neuroanatomical differences that have been reported in the literature. However, phylogenetic comparative methods have not yet been used to map the evolution of neuroanatomical traits in bonobos and chimpanzees, limiting our ability to understand which neural systems are derived in each species in relation to the last common ancestor of Pan (Pan-LCA). Here, we examine evolutionary changes in neuroanatomical traits of bonobos and chimpanzees relative to ancestral character reconstructions of the Pan-LCA using comparative datasets from hominoids. We found that bonobo brains are derived in showing reduction of whole brain and white matter volumes, with particularly striking reduction of male brain size compared to the inferred Pan-LCA value. Brain structures related to social cognition and emotional regulation, like the insular cortex and amygdala, display a mosaic pattern of evolution with certain traits changing to a greater extent in each species. Examination of potential genetic mechanisms underlying divergence of neural and social traits did not reveal clear differences in protein evolution patterns between the two species. These findings suggest that the brain anatomy of extant bonobos and chimpanzees show lineage-specific specializations and neither can be considered to more closely retain the ancestral state of Pan. Consequently, this raises questions about the extent that modern chimpanzees or bonobos may serve as referential models for the neuroanatomy of the LCA of humans and apes., (Copyright © 2018. Published by Elsevier Ltd.)
- Published
- 2019
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23. Evolution of ASPM coding variation in apes and associations with brain structure in chimpanzees.
- Author
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Singh SV, Staes N, Guevara EE, Schapiro SJ, Ely JJ, Hopkins WD, Sherwood CC, and Bradley BJ
- Subjects
- Animals, Brain anatomy & histology, Female, Male, Pan paniscus genetics, Brain diagnostic imaging, Evolution, Molecular, Microtubule-Associated Proteins genetics, Nerve Tissue Proteins genetics, Pan troglodytes genetics, Polymorphism, Genetic
- Abstract
Studying genetic mechanisms underlying primate brain morphology can provide insight into the evolution of human brain structure and cognition. In humans, loss-of-function mutations in the gene coding for ASPM (Abnormal Spindle Microtubule Assembly) have been associated with primary microcephaly, which is defined by a significantly reduced brain volume, intellectual disability and delayed development. However, less is known about the effects of common ASPM variation in humans and other primates. In this study, we characterized the degree of coding variation at ASPM in a large sample of chimpanzees (N = 241), and examined potential associations between genotype and various measures of brain morphology. We identified and genotyped five non-synonymous polymorphisms in exons 3 (V588G), 18 (Q2772K, K2796E, C2811Y) and 27 (I3427V). Using T1-weighted magnetic resonance imaging of brains, we measured total brain volume, cerebral gray and white matter volume, cerebral ventricular volume, and cortical surface area in the same chimpanzees. We found a potential association between ASPM V588G genotype and cerebral ventricular volume but not with the other measures. Additionally, we found that chimpanzee, bonobo, and human lineages each independently show a signature of accelerated ASPM protein evolution. Overall, our results suggest the potential effects of ASPM variation on cerebral cortical development, and emphasize the need for further functional studies. These results are the first evidence suggesting ASPM variation might play a role in shaping natural variation in brain structure in nonhuman primates., (© 2019 John Wiley & Sons Ltd and International Behavioural and Neural Genetics Society.)
- Published
- 2019
- Full Text
- View/download PDF
24. Serotonin Receptor 1A Variation Is Associated with Anxiety and Agonistic Behavior in Chimpanzees.
- Author
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Staes N, Sherwood CC, Freeman H, Brosnan SF, Schapiro SJ, Hopkins WD, and Bradley BJ
- Subjects
- Amino Acid Sequence, Animals, Female, Genetic Variation, Male, Pan troglodytes psychology, Personality genetics, Agonistic Behavior, Anxiety genetics, Pan troglodytes genetics, Receptor, Serotonin, 5-HT1A genetics
- Abstract
Serotonin is a neurotransmitter that plays an important role in regulating behavior and personality in humans and other mammals. Polymorphisms in genes coding for the serotonin receptor subtype 1A (HTR1A), the serotonin transporter (SLC6A4), and the serotonin degrading enzyme monoamine oxidase A (MAOA) are associated with anxiety, impulsivity, and neurotic personality in humans. In primates, previous research has largely focused on SLC6A4 and MAOA, with few studies investigating the role of HTR1A polymorphic variation on behavior. Here, we examined variation in the coding region of HTR1A across apes, and genotyped polymorphic coding variation in a sample of 214 chimpanzees with matched measures of personality and behavior. We found evidence for positive selection at three amino acid substitution sites, one in chimpanzees-bonobos (Thr26Ser), one in humans (Phe33Val), and one in orangutans (Ala274Gly). Investigation of the HTR1A coding region in chimpanzees revealed a polymorphic site, where a C/A single nucleotide polymorphism changes a proline to a glutamine in the amino acid sequence (Pro248Gln). The substitution is located in the third intracellular loop of the receptor, a region important for serotonin signal transduction. The derived variant is the major allele in this population (frequency 0.67), and is associated with a reduction in anxiety, decreased rates of male agonistic behavior, and an increase in socio-positive behavior. These results are the first evidence that the HTR1A gene may be involved in regulating social behavior in chimpanzees and encourage further systematic investigation of polymorphic variation in other primate populations with corresponding data on behavior., (© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)
- Published
- 2019
- Full Text
- View/download PDF
25. Comparison of bonobo and chimpanzee brain microstructure reveals differences in socio-emotional circuits.
- Author
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Issa HA, Staes N, Diggs-Galligan S, Stimpson CD, Gendron-Fitzpatrick A, Taglialatela JP, Hof PR, Hopkins WD, and Sherwood CC
- Subjects
- Animals, Biomarkers metabolism, Brain metabolism, Female, Male, Neural Pathways anatomy & histology, Neural Pathways metabolism, Neuropil metabolism, Pan paniscus metabolism, Pan paniscus psychology, Pan troglodytes metabolism, Pan troglodytes psychology, Species Specificity, Behavior, Animal, Brain anatomy & histology, Emotions, Pan paniscus anatomy & histology, Pan troglodytes anatomy & histology, Social Behavior
- Abstract
Despite being closely related, bonobos and chimpanzees exhibit several behavioral differences. For instance, studies indicate that chimpanzees are more aggressive, territorial, and risk-taking, while bonobos exhibit greater social tolerance and higher rates of socio-sexual interactions. To elucidate the potential neuroanatomical variation that accompanies these differences, we examined the microstructure of selected brain areas by quantifying the neuropil fraction, a measure of the relative tissue area occupied by structural elements of connectivity (e.g., dendrites, axons, and synapses) versus cell bodies. In bonobos and chimpanzees, we compared neuropil fractions in the nucleus accumbens (NAc; core and shell), amygdala (whole, accessory basal, basal, central and lateral nuclei), anterior cingulate cortex (ACC; dorsal and subgenual), anterior insular cortex (AIC), and primary motor cortex (M1). In the dorsal ACC and frontoinsular cortex (FI) we also quantified numbers of von Economo neurons (VENs), a unique subset of neurons thought to be involved in rapid information processing during social interactions. We predicted that the neuropil fraction and number of VENs in brain regions associated with socio-emotional processing would be higher in bonobos. In support of this hypothesis, we found that bonobos had significantly greater neuropil in the central and accessory basal nuclei of the amygdala, as well as layers V-VI of the subgenual ACC. However, we did not find a difference in the numbers of VENs between the two species. These findings support the conclusion that bonobo and chimpanzee brains differ in the anatomical organization of socio-emotional systems that may reflect species-specific variation in behavior.
- Published
- 2019
- Full Text
- View/download PDF
26. FOXP2 variation in great ape populations offers insight into the evolution of communication skills.
- Author
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Staes N, Sherwood CC, Wright K, de Manuel M, Guevara EE, Marques-Bonet T, Krützen M, Massiah M, Hopkins WD, Ely JJ, and Bradley BJ
- Subjects
- Amino Acid Sequence, Animals, Biological Evolution, Forkhead Transcription Factors chemistry, Forkhead Transcription Factors metabolism, Gene Frequency, Gorilla gorilla genetics, Hominidae, Microsatellite Repeats genetics, Pan paniscus genetics, Pan troglodytes genetics, Polymorphism, Single Nucleotide, Pongo abelii genetics, Pongo pygmaeus genetics, Protein Structure, Secondary, Sequence Alignment, Forkhead Transcription Factors genetics, Genetic Variation, Vocalization, Animal physiology
- Abstract
The gene coding for the forkhead box protein P2 (FOXP2) is associated with human language disorders. Evolutionary changes in this gene are hypothesized to have contributed to the emergence of speech and language in the human lineage. Although FOXP2 is highly conserved across most mammals, humans differ at two functional amino acid substitutions from chimpanzees, bonobos and gorillas, with an additional fixed substitution found in orangutans. However, FOXP2 has been characterized in only a small number of apes and no publication to date has examined the degree of natural variation in large samples of unrelated great apes. Here, we analyzed the genetic variation in the FOXP2 coding sequence in 63 chimpanzees, 11 bonobos, 48 gorillas, 37 orangutans and 2 gibbons and observed undescribed variation in great apes. We identified two variable polyglutamine microsatellites in chimpanzees and orangutans and found three nonsynonymous single nucleotide polymorphisms, one in chimpanzees, one in gorillas and one in orangutans with derived allele frequencies of 0.01, 0.26 and 0.29, respectively. Structural and functional protein modeling indicate a biochemical effect of the substitution in orangutans, and because of its presence solely in the Sumatran orangutan species, the mutation may be associated with reported population differences in vocalizations.
- Published
- 2017
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27. Bonobo personality traits are heritable and associated with vasopressin receptor gene 1a variation.
- Author
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Staes N, Weiss A, Helsen P, Korody M, Eens M, and Stevens JMG
- Subjects
- Animals, Female, Male, Pan paniscus genetics, Personality genetics, Polymorphism, Genetic, Quantitative Trait, Heritable, Receptors, Vasopressin genetics
- 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 (Sociability
B , 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.- Published
- 2016
- Full Text
- View/download PDF
28. Personality in Bonobos.
- Author
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Weiss A, Staes N, Pereboom JJ, Inoue-Murayama M, Stevens JM, and Eens M
- Subjects
- Animals, Biological Evolution, Female, Male, Phylogeny, Behavior, Animal, Pan paniscus psychology, Pan troglodytes psychology, Personality
- Abstract
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., (© The Author(s) 2015.)
- Published
- 2015
- Full Text
- View/download PDF
29. Chimpanzee sociability is associated with vasopressin (Avpr1a) but not oxytocin receptor gene (OXTR) variation.
- Author
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Staes N, Koski SE, Helsen P, Fransen E, Eens M, and Stevens JM
- Subjects
- Alleles, Animals, Female, Male, Oxytocin genetics, Pan troglodytes genetics, Polymorphism, Single Nucleotide, Promoter Regions, Genetic, Pan troglodytes psychology, Personality genetics, Receptors, Oxytocin genetics, Receptors, Vasopressin genetics, Social Behavior
- Abstract
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., (Copyright © 2015 Elsevier Inc. All rights reserved.)
- Published
- 2015
- Full Text
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30. Oxytocin and vasopressin receptor gene variation as a proximate base for inter- and intraspecific behavioral differences in bonobos and chimpanzees.
- Author
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Staes N, Stevens JM, Helsen P, Hillyer M, Korody M, and Eens M
- Subjects
- Alleles, Animals, Base Sequence, Female, Gene Frequency, Genotype, Humans, Male, Microsatellite Repeats genetics, Molecular Sequence Data, Pan paniscus, Pan troglodytes, Sequence Homology, Nucleic Acid, Polymorphism, Single Nucleotide, Receptors, Oxytocin genetics, Receptors, Vasopressin genetics, Social Behavior
- Abstract
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.
- Published
- 2014
- Full Text
- View/download PDF
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