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

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          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.

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          The bonobo genome compared with the chimpanzee and human genomes.

          Two African apes are the closest living relatives of humans: the chimpanzee (Pan troglodytes) and the bonobo (Pan paniscus). Although they are similar in many respects, bonobos and chimpanzees differ strikingly in key social and sexual behaviours, and for some of these traits they show more similarity with humans than with each other. Here we report the sequencing and assembly of the bonobo genome to study its evolutionary relationship with the chimpanzee and human genomes. We find that more than three per cent of the human genome is more closely related to either the bonobo or the chimpanzee genome than these are to each other. These regions allow various aspects of the ancestry of the two ape species to be reconstructed. In addition, many of the regions that overlap genes may eventually help us understand the genetic basis of phenotypes that humans share with one of the two apes to the exclusion of the other.
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            Tolerance allows bonobos to outperform chimpanzees on a cooperative task.

            To understand constraints on the evolution of cooperation, we compared the ability of bonobos and chimpanzees to cooperatively solve a food-retrieval problem. We addressed two hypotheses. The "emotional-reactivity hypothesis" predicts that bonobos will cooperate more successfully because tolerance levels are higher in bonobos. This prediction is inspired by studies of domesticated animals; such studies suggest that selection on emotional reactivity can influence the ability to solve social problems [1, 2]. In contrast, the "hunting hypothesis" predicts that chimpanzees will cooperate more successfully because only chimpanzees have been reported to cooperatively hunt in the wild [3-5]. We indexed emotional reactivity by measuring social tolerance while the animals were cofeeding and found that bonobos were more tolerant of cofeeding than chimpanzees. In addition, during cofeeding tests only bonobos exhibited socio-sexual behavior, and they played more. When presented with a task of retrieving food that was difficult to monopolize, bonobos and chimpanzees were equally cooperative. However, when the food reward was highly monopolizable, bonobos were more successful than chimpanzees at cooperating to retrieve it. These results support the emotional-reactivity hypothesis. Selection on temperament may in part explain the variance in cooperative ability across species, including hominoids.
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              Microsatellite instability generates diversity in brain and sociobehavioral traits.

              Repetitive microsatellites mutate at relatively high rates and may contribute to the rapid evolution of species-typical traits. We show that individual alleles of a repetitive polymorphic microsatellite in the 5' region of the prairie vole vasopressin 1a receptor (avpr1a) gene modify gene expression in vitro. In vivo, we observe that this regulatory polymorphism predicts both individual differences in receptor distribution patterns and socio-behavioral traits. These data suggest that individual differences in gene expression patterns may be conferred via polymorphic microsatellites in the cis-regulatory regions of genes and may contribute to normal variation in behavioral traits.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                18 November 2014
                : 9
                : 11
                : e113364
                Affiliations
                [1 ]University of Antwerp, Department of Biology, Ethology research group, 2610, Antwerp, Belgium
                [2 ]Centre for Research and Conservation, Royal Zoological Society of Antwerp, 2018, Antwerp, Belgium
                [3 ]San Diego Zoo Institute for Conservation Research, Escondido, CA 92027, United States of America
                [4 ]Molecular Systematics Unit, Western Australian Museum, Perth, WA 6106, Australia
                Oregon Health and Science University, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NS JMGS. Performed the experiments: NS MH MK PH. Analyzed the data: NS PH MH. Contributed reagents/materials/analysis tools: PH MK. Contributed to the writing of the manuscript: NS JMGS PH MH MK ME.

                Article
                PONE-D-14-17755
                10.1371/journal.pone.0113364
                4236177
                25405348
                1d2b496b-3e30-4b91-ba07-af03a3f03adf
                Copyright @ 2014

                This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 5 June 2014
                : 22 October 2014
                Page count
                Pages: 9
                Funding
                Funds for this study come from the Flemish government, who provides structural support of the CRC of the RSZA, FWO Flanders and the University of Antwerp. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biochemistry
                Hormones
                Peptide Hormones
                Oxytocin
                Vasopressin
                Evolutionary Biology
                Evolutionary Genetics
                Neuroscience
                Behavioral Neuroscience
                Zoology
                Mammalogy
                Primatology
                Animal Behavior
                Custom metadata
                The authors confirm that all data underlying the findings are fully available without restriction. All newly identified SNP sequences are available from the NCBI database (accession numbers ss1388116469, ss1388116470, ss1388116471, ss1388116472, ss1388116473).

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                Uncategorized

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