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Distributions of Oxytocin and Vasopressin 1A Distributions of oxytocin and vasopressin 1a receptors in the Taiwan vole and their role in social monogamy A.R Chappell, University of Louisiana Monroe S.M Freeman, Emory University Y.K Lin, National Taiwan University Jamie LaPrairie, Emory University K. Inoue, Emory University Larry Young, Emory University LD Hayes, University of Louisiana Monroe Journal Title: Journal of Zoological Systematics and Evolutionary Research Volume: Volume 299, Number 2 Publisher: Wiley | 2016-06-01, Pages 106-115 Type of Work: Article | Post-print: After Peer Review Publisher DOI: 10.1111/jzo.12332 Permanent URL: https://pid.emory.edu/ark:/25593/s30qw Final published version: http://dx.doi.org/10.1111/jzo.12332 Copyright information: © 2016 The Zoological Society of London.This is the peer reviewed version of the following article, which has been published in final form. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving. Accessed October 2, 2021 12:48 PM EDT HHS Public Access Author manuscript Author ManuscriptAuthor Manuscript Author J Zool (1987) Manuscript Author . Author manuscript; Manuscript Author available in PMC 2017 June 01. Published in final edited form as: J Zool (1987). 2016 June ; 299(2): 106–115. doi:10.1111/jzo.12332. Distributions of oxytocin and vasopressin 1a receptors in the Taiwan vole and their role in social monogamy A. R. Chappell1, S. M. Freeman2,3, Y. K. Lin4, J. L. LaPrairie2, K. Inoue2, L. J. Young2, and L. D. Hayes1,5 1Department of Biology, University of Louisiana at Monroe, Monroe, LA 71209, USA 2Silvio O. Conte Center for Oxytocin and Social Cognition, Center for Translational Social Neuroscience, Department of Psychiatry and Behavioral Sciences, Yerkes National Primate Research Center, Emory University, Atlanta, GA, 30329, USA 3California National Primate Research Center, University of California-Davis, Davis, CA 95616, USA 4Department of Life Science, College of Life Science, National Taiwan University, Taipei, Taiwan 5Department of Biological and Environmental Sciences, University of Tennessee at Chattanooga, Chattanooga, TN 37403, USA Abstract Social monogamy is a mating strategy rarely employed by mammalian species. Laboratory studies in socially monogamous prairie voles (Microtus ochrogaster) demonstrate that oxytocin and vasopressin act within the mesolimbic dopamine pathway to facilitate pair-bond formation. Species differences in oxytocin receptor (OTR) and vasopressin 1a receptor (V1aR) distribution in this pathway are associated with species differences in mating strategy. Here we characterize the neuroanatomical distribution of OTR and V1aR binding sites in naturally occurring populations of Taiwan voles (M. kikuchii), which purportedly display social monogamy. Live trapping was conducted at two sites in 2009–2010 and receptor autoradiography for OTR and V1aR was performed on brains from 24 animals. OTR binding in two brain regions where OTR signaling regulates pair-bonding were directly compared with that of prairie voles. Our results show that like prairie voles, Taiwan voles exhibit OTR in the prefrontal cortex, insular cortex, claustrum, nucleus accumbens, caudate-putamen, dorsal lateral septal nucleus, central amygdala, and ventromedial hypothalamus. Unlike prairie voles, Taiwan voles exhibit OTR binding in the CA3 pathway of the hippocampus, as well as the indusium griseum, which has only previously been documented in tuco-tucos (Ctenomys haigi, C. sociabilis), Syrian hamsters (Mesocricetus auratus) and naked mole-rats (Heterocephalus glaber). V1aR binding was present in the ventral pallidum, lateral septum, nucleus basalis, bed nucleus of the stria terminalis, hippocampus, medial amygdala, and anterior, ventromedial and dorsomedial hypothalamus. Marked individual differences in V1aR binding were noted in the cingulate cortex and several thalamic nuclei, remarkably similar to prairie voles. While pharmacological studies are needed to determine whether oxytocin and Correspondence: Loren D. Hayes, Department of Biological and Environmental Sciences, University of Tennessee at Chattanooga, Chattanooga, TN 37403, USA. [email protected]. Chappell et al. Page 2 vasopressin are involved in pair-bond formation in this species, our results lay a foundation for Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author future investigations into the role of these neuropeptides in Taiwan vole social behavior. Keywords Oxytocin; vasopressin; neuropeptide distribution; mating systems; social monogamy; vole; pairing; social behaviour INTRODUCTION Social mating systems vary widely across vertebrate species. Social monogamy refers to the condition where one male lives in association with only one female. The prevalence of social monogamy across vertebrates varies considerably, with approximately 90% of bird species forming partnerships that endure at least one breeding season (Lack, 1968) and 400 of over 3000 African cichlid species exhibiting biparental brood care (an indicator of social monogamy; Perrone, 1978). In contrast, monogamy is rare in reptiles (While, Uller & Wapstra, 2009) and amphibians (Gillette, Jaeger, & Peterson, 2000). Estimates suggest only 5% of mammalian species exhibit social monogamy, with genetic monogamy being even less common (Lukas & Clutton-Brock, 2012). The neuropeptides oxytocin (OT) and vasopressin (AVP) play important roles in several aspects of species-typical social behaviors, including those related to monogamy (Young & Wang, 2004; Oldfield & Hofmann, 2011; Johnson & Young, 2015). OT, AVP, and their nonmammalian homologues modulate a variety of social behaviors relevant to mating strategies, including parental and alloparental care (Olazábal & Young, 2006; Rilling & Young, 2014), territorial behavior and aggression (Albers, 2012), vocal communications (Goodson, Evans & Bass, 2003), flocking (Goodson et al., 2009) and pair-bonding (Young & Wang, 2004). Much of our understanding of neural control of mammalian social mating systems comes from laboratory work on voles (Lim et al., 2004b; Young & Wang, 2004; Johnson & Young, 2015). Socially monogamous prairie voles (Microtus ochrogaster) have relatively high concentrations of oxytocin receptors (OTR) and vasopressin 1a receptors (V1aR) in the reward and reinforcement regions of the brain, namely OTR in the nucleus accumbens (NAcc) and prefrontal cortex (PFC) and V1aR in the ventral pallidum (VP). In contrast, non- monogamous voles, such as montane (M. montanus) and meadow voles (M. pennsylvanicus), have low OTR in the NAcc and low V1aR in the VP. Administration of an OTR antagonist into the PFC or NAcc or infusion of a V1aR antagonist into the VP prevent mating-induced partner-preference formation, a proxy of the pair-bond (Young et al., 2001; Lim & Young, 2004). Thus, species differences in OTR and V1aR in the NAcc and VP, respectively, may underlie differences in pair-bonding between prairie and meadow voles. Increasing V1aR density in the VP of male meadow vole brains resulted in the display of partner-preferences, providing evidence for a causal link between receptor expression and pair-bonding (Lim et al., 2004b). Receptor density can also vary between individuals, contributing to individual differences in social behavior and providing a potential mechanism for creating different sociosexual phenotypes, which can then shape species’ mating systems through natural selection (Olazábal & Young, 2006; Ross et al., 2009; J Zool (1987). Author manuscript; available in PMC 2017 June 01. Chappell et al. Page 3 Barrett, Arambula & Young, 2015). Individual variation in V1aR and OTR density in prairie Author ManuscriptAuthor Manuscript Author Manuscript Author Manuscript Author voles have been linked to genetic polymorphisms in the respective genes (Hammock & Young, 2005; King et al., 2016). These observations suggest intraspecific variation in mating systems, as seen in some mammals (Cushing et al., 2001; Bales et al., 2007), may be influenced by the distribution of neuropeptide receptors in the brain (Solomon et al., 2009; Ophir et al., 2012). However, male prairie voles from Illinois and Kansas vary in their display of monogamous behaviors: Illinois males are more behaviorally sensitive to AVP, yet these populations do not differ in V1aR binding in the brain (Cushing et al., 2001). Thus, while neuropeptide receptor expression in particular brain regions may be associated with variation in mating strategy, receptor density alone cannot predict behavioral patterns across populations. The objective of this study was to characterize OTR and V1aR distributions in the Taiwan vole (M. kikuchii) brain, a rodent endemic to high elevation (3000m) meadows and forests in central Taiwan (Yu, 1994); sites which may be immediately adjacent to one another, but are characterized by different vegetative composition and structure. While little is known about behavioral differences exhibited between habitats in this species, ecology is an important factor in predicting mating system variation across taxa, both interspecifically (Emlen & Oring, 1977; Schamel et al., 2004) and intraspecifically (Cushing et al., 2001; Brashares & Arcese, 2002; Streatfeild et al., 2011). Thus, we hypothesized that intraspecific ecological variation could also select for differences in mating strategy which could be reflected in OTR and V1aR distributions in Taiwan voles from different habitats. Specifically, we hypothesized that when female dispersion is high, as would be predicted
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