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Differential Functional Variability of Serotonin Transporter and Monoamine Oxidase A Genes in Macaque Species Displaying Contrasting Levels of Aggression-Related Behavior

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Abstract

Functional allelic variation in the transcriptional control region of the serotonin transporter and monoamine oxidase A genes has been associated with anxiety- and aggression-related behavior in humans and, more recently, in nonhuman primates. Here, we have genotyped these polymorphic regions in seven species of the genus Macaca. Macaques exhibit exceptional inter-species variation in aggression-related social behavior as illustrated by recent studies showing overlapping patterns of aggression-based social organization grades and macaque phylogeny. We cloned and sequenced two new alleles of the serotonin transporter gene-linked polymorphic region in Barbary and Tibetan macaques. In addition, we observed that species displaying tolerant societies, with relaxed dominance and high levels of conciliatory tendency, were monomorphic for both the serotonin transporter gene and, with the exception of Tonkean macaques, the monoamine oxidase A gene. In contrast, those species known to exhibit intolerant, hierarchical and nepotistic societies were polymorphic at one or more of these loci. Rhesus (M. mulatta), the most intolerant and hierarchical species of macaques, showed the greatest degree of allelic variation in both genes. Additional investigation of a polymorphic repeat in exon III of the dopamine receptor D4 as well as a repeat/single nucleotide polymorphism in the 3′ untranslated region of the dopamine transporter which have both been implicated in the modulation of complex behavior failed to reveal a relationship between allelic variability and social organization grade. Taken together, these findings suggest that genetic variation of serotonergic neurotransmission may play an important role in determining inter-species differences in aggression related behavior in macaques.

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ACKNOWLEDGMENTS

The authors thank Gabriela Ortega, Nicole Steigerwald and Mukta Kundu for excellent technical assistance in blood and DNA sample processing, genotyping, cloning and data collection. We are greatly indebted to G. Flügge, Deutsches Primatenzentrum, Göttingen, Germany; I. den Hartog and E. van Lavieren, AAP Sanctuary for Exotic Animals, Almere, The Netherlands; A. Johann, Naturzoo Rheine, Germany; G. de Tuerkheim, E. Merz and W. Angst, Affenberg Salem, Germany; S. Bost and D. Reichle, Wildpark Daun, Germany; and CIBA Vision, Strasbourg, France, for providing blood samples of different macaque species. Supported by the Division of Intramural Research, National Institute of Child Health & Human Development, National Institutes of Health and the European Commission (NEWMOOD LSHM-CT-2003–503474) and the Deutsche Forschungsgemeinschaft (SFB 581, KFO 125/1–1).

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Authors and Affiliations

  1. Clinical and Molecular Psychobiology, Department of Psychiatry and Psychotherapy, University of Würzburg, 97080, Würzburg, Germany

    Jens R. Wendland & Klaus-Peter Lesch

  2. National Institute on Alcohol Abuse and Alcoholism, Laboratory of Clinical Studies-Primate Unit, Poolesville, MD, 20837, USA

    Timothy K. Newman

  3. Institute of Human Biology and Anthropology, Freie Universität Berlin, 14195, Berlin, Germany

    Angelika Timme

  4. Centre d’Ecologie et Physiologie Energétiques, Centre National pour la Recherche Scientifique, Strasbourg, France

    Hélène Gachot-Neveu & Bernard Thierry

  5. National Institute on Child Health and Human Development, Laboratory of Comparative Ethology, Poolesville, MD, 20837, USA

    Stephen J. Suomi

  6. Laboratory of Clinical Science, National Institute of Mental Health, 10 Center Dr.; Bldg. 10, Rm. 3D41, Bethesda, MD, 20892-1264, USA

    Jens R. Wendland

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  1. Jens R. Wendland
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  2. Klaus-Peter Lesch
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  3. Timothy K. Newman
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  4. Angelika Timme
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Correspondence to Jens R. Wendland.

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Wendland, J., Lesch, KP., Newman, T. et al. Differential Functional Variability of Serotonin Transporter and Monoamine Oxidase A Genes in Macaque Species Displaying Contrasting Levels of Aggression-Related Behavior. Behav Genet 36, 163–172 (2006). https://doi.org/10.1007/s10519-005-9017-8

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