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AVPR1A Sequence Variation in Monogamous Owl Monkeys (Aotus Azarai) and Its Implications for the Evolution of Platyrrhine Social Behavior

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AVPR1A Sequence Variation in Monogamous Owl Monkeys (Aotus Azarai) and Its Implications for the Evolution of Platyrrhine Social Behavior ISSN 0022-2844, Volume 71, Number 4 This article was published in the above mentioned Springer issue. The material, including all portions thereof, is protected by copyright; all rights are held exclusively by Springer Science + Business Media. The material is for personal use only; commercial use is not permitted. Unauthorized reproduction, transfer and/or use may be a violation of criminal as well as civil law. J Mol Evol (2010) 71:279–297 Author's personal copy DOI 10.1007/s00239-010-9383-6 AVPR1A Sequence Variation in Monogamous Owl Monkeys (Aotus azarai) and Its Implications for the Evolution of Platyrrhine Social Behavior Paul L. Babb • Eduardo Fernandez-Duque • Theodore G. Schurr Received: 29 December 2009 / Accepted: 17 August 2010 / Published online: 14 September 2010 Ó Springer Science+Business Media, LLC 2010 Abstract The arginine vasopressin V1a receptor gene Keywords Behavioral genetics Á Monogamy Á V1aR Á (AVPR1A) has been implicated in increased partner pref- Vasopressin Á Primates erence and pair bonding behavior in mammalian lineages. This observation is of considerable importance for studies of social monogamy, which only appears in a small subset Introduction of primate taxa, including the Argentinean owl monkey (Aotus azarai). Thus, to investigate the possible influence Primate species exhibit an extensive range of social of AVPR1A on the evolution of social behavior in owl behaviors and, as a result, display considerable diversity in monkeys, we sequenced this locus in a wild population their social organization and reproductive strategies, from the Gran Chaco. We also assessed the interspecific including social monogamy. Owl monkeys (Aotus spp.), variation of AVPR1A in platyrrhine species that represent a saki monkeys (Pithecia spp.), and titi monkeys (Callicebus set of phylogenetically and behaviorally disparate taxa. spp.) exemplify the minority of primate species living in The resulting data revealed A. azarai to have a unique small social groups (Kleiman 1977; Wright 1994; Van genic structure for AVPR1A that varies in coding sequence Schaik and Kappeler 2003). These particular platyrrhines, and microsatellite repeat content relative to other primate or New World monkeys, along with other taxa such as the and mammalian species. Specifically, one repetitive region indris, fat-tailed dwarf lemurs, callitrichids, and gibbons, that has been the focus in studies of human AVPR1A are traditionally defined as possessing prolonged and diversity, ‘‘RS3,’’ is completely absent in A. azarai and all essentially exclusive mating relationship between one male other platyrrhines examined. This finding suggests that, if and one female, which comprise the basic social unit AVPR1A modulates behavior in owl monkeys and other (Kleiman 1977; Mock and Fujioka 1990; Palombit 1994). neotropical primates, it does so independent of this region. Such monogamous social systems are rare among primates, These observations have also provided clues about the but are widely distributed across the order, indicating that process by which the range of social behavior in the Order they have arisen independently multiple times (van Shaik Primates evolved through lineage-specific neurogenetic and van Hoof 1983; van Schaik and Dunbar 1990). variation. Although ‘‘monogamy’’ necessarily involves many differ- ent complex behaviors (Mendoza et al. 2002; Moller 2003), this scenario raises an important question: are the social behaviors of primates controlled by the same genes in different species? By comparing genetic regions that are P. L. Babb Á E. Fernandez-Duque Á T. G. Schurr (&) Department of Anthropology, University of Pennsylvania, related to these behaviors across primate taxa, one can 344 University Museum, 3260 South Street, Philadelphia, begin to determine whether the evolution of complex social PA 19104-6398, USA behavior occurs through conserved molecular mechanisms. e-mail: [email protected] Current research on voles (Microtus spp.) and other E. Fernandez-Duque mammals suggests that variation at key neurogenetic loci CECOAL-Conicet, Corrientes, Argentina likely played an important role in the evolution of social 123 280 Author's personal copy J Mol Evol (2010) 71:279–297 behavior at both inter- and intraspecific levels (Lim et al. variation (Donaldson et al. 2008; Rosso et al. 2008). These 2004a). In voles and other rodents, the hormone arginine differences consist of numerous amino acid changes that vasopressin (AVP) and the V1a receptor protein (V1aR, have accumulated in different taxa, as well as lineage- encoded by the gene AVPR1A) are implicated in the vari- specific STR motifs and length distributions (Fig. 1). It has able expression of pair bonding in both sexes. This is a been suggested that different aspects of these variable necessary behavioral component for the manifestation of components in or surrounding AVPR1A have been involved monogamous social systems (Young et al. 1999; Hammock in the evolution of different primate social systems (Don- and Young 2002; Turner et al. 2010). However, AVP has aldson et al. 2008; Rosso et al. 2008). However, despite the directly been linked to a variety of crucial processes in diversity of social behaviors observed in platyrrhine pri- mammals, ranging from the regulation of circadian mates, including the apparent enrichment of monogamous rhythms, fluid retention, and the vasoconstriction of blood social systems, there have been no studies of AVPR1A vessels (Thibonnier et al. 1996). The fact that AVP is sequence variation in these species. pleiotropic in its effects complicates efforts to link For this reason, we began exploring the molecular evo- sequence variation at this locus to behavioral phenotypes. lution of AVPR1A in New World primates to clarify its Variation in the expression and localization of V1aR possible role in the evolution of their mating behavior and proteins also influences the manifestation of pair bonding social organization. We initially sequenced the entire in mammalian species. The differential neuroanatomical AVPR1A locus in a wild population of monogamous owl distribution of V1aR G-protein-coupled receptor (GPCR) monkeys (Aotus azarai) to characterize the genetic variation proteins functionally distinguishes monogamous prairie present in the 50 promoter and coding region at the intra- voles (Microtus ochrogaster) from their polygynous rela- specific level. We then sequenced AVPR1A in several plat- tives (Pitkow et al. 2001). In addition, viral vector-medi- yrrhine taxa exhibiting a range of mating systems to assess ated transfers of the AVPR1A gene into the ventral interspecific levels of genetic variation. We anticipated that forebrain of polygynous meadow voles (Microtus penn- the AVPR1A gene of owl monkeys and other platyrrhines sylvanicus) demonstrated a significant increase in their would exhibit species-specific coding region substitutions likelihood to exhibit a partner preference (Lim et al. 2004a, relative to other primate taxa, and that these variants could b), whereas a separate study using in vitro expression lead to novel structural characteristics of their V1aR pro- assays have revealed that inter- and intraspecific differ- teins. In addition, intraspecific variation of STRs present in ences in short tandem repeat (STR) length influence the 50 region of the owl monkey AVPR1A were expected to AVPR1A expression (Hammock and Young 2004, 2005). exhibit a range of allele sizes that would be commensurate Differences in V1aR density and localization in the brains with those seen in previous genotyping surveys of primate of different mammalian taxa are also associated with spe- populations (Donaldson et al. 2008; Rosso et al. 2008). cific lengths of microsatellite STRs found in the 50 Our results reveal novel patterns of genetic variation upstream promoter region AVPR1A, and are positively among platyrrhine primates, and show that this variation correlated with the expression of the gene in a tissue-spe- distinguishes them from their Old World relatives. These cific manner (Hammock and Young 2002, 2004, 2005; findings suggest that if monogamy has indeed evolved Hammock et al. 2005; Young et al. 2005; Young and independently in primates on both sides of the Atlantic, Hammock 2007). Overall, these studies demonstrate that then it may have done so through different molecular the distribution of V1aR in the brain directly influences mechanisms. social behavior. They further suggest that the evolution of regulatory sequences drives the expression of the gene, and may be Methods responsible for emergence of different social structures in different species. However, STR patterns are not the only Study Population component responsible for differences in brain expression of AVPR1A. As noted by Fink et al. (2006), this pattern is Azara’s owl monkeys, A. azarai, inhabit the gallery forests more of a phylogenetic oddity than a consistent pattern and the patchy forest-islands interspersed throughout the related to monogamy versus polygamy. Instead, amino acid savannahs of northeastern Argentina. Their social groups changes in the coding region of AVPR1A may explain so- are small (two to six individuals), being comprised of an ciobehavioral differences across species (Fink et al. 2007; adult heterosexual pair, one infant, and one or two juve- Phelps et al. 2009; Turner et al. 2010). niles, and occasionally a subadult (Rotundo et al. 2005; In this regard, recent work tracing the sequence evolu- Fernandez-Duque 2009). The adult male in the group is tion of AVPR1A in catarrhine
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