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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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Abstract

The arginine vasopressin V1a receptor gene (AVPR1A) has been implicated in increased partner preference 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 of primate taxa, including the Argentinean owl monkey (Aotus azarai). Thus, to investigate the possible influence of AVPR1A on the evolution of social behavior in owl monkeys, we sequenced this locus in a wild population from the Gran Chaco. We also assessed the interspecific variation of AVPR1A in platyrrhine species that represent a set of phylogenetically and behaviorally disparate taxa. The resulting data revealed A. azarai to have a unique genic structure for AVPR1A that varies in coding sequence and microsatellite repeat content relative to other primate and mammalian species. Specifically, one repetitive region that has been the focus in studies of human AVPR1A diversity, “RS3,” is completely absent in A. azarai and all other platyrrhines examined. This finding suggests that, if AVPR1A modulates behavior in owl monkeys and other neotropical primates, it does so independent of this region. These observations have also provided clues about the process by which the range of social behavior in the Order Primates evolved through lineage-specific neurogenetic variation.

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References

  • Altekar G, Dwarkadas S, Huelsenbeck JP, Ronquist F (2004) Parallel metropolis-coupled Markov Chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20:407–415

    Article  CAS  PubMed  Google Scholar 

  • Bandelt HJ, Parson W (2008) Consistent treatment of length variants in the human mtDNA control region: a reappraisal. Int J Legal Med 122:11–21

    Article  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Sykes BC, Richards MB (1995) Mitochondrial portraits of human populations. Genetics 141:743–753

    CAS  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  • Bandelt HJ, Macaulay V, Richards M (2000) Median networks: speedy construction and greedy reduction, one simulation, and two case studies from human mtDNA. Mol Phylogenet Evol 16:8–28

    Article  CAS  PubMed  Google Scholar 

  • Bandelt HJ, Quintana-Murci L, Salas A, Macaulay V (2002) The fingerprint of phantom mutations in mitochondrial DNA data. Am J Hum Genet 71:1150–1160

    Article  CAS  PubMed  Google Scholar 

  • Bell SD, Magill CP, Jackson SP (2001) Basal and regulated transcription in Archaea. Biochem Soc Trans 29(4):392–395

    Article  CAS  PubMed  Google Scholar 

  • Boinski S (1999) The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evol Anthropol 8(3):101–114

    Article  Google Scholar 

  • Conrad D, Pinto D, Redon R, Feuk L, Gökçümen Ö, Zhang Y, Aerts J, Andrews TD, Barnes C, Campbell P, Fitzgerald T, Hu M, Ihm CH, Kristiansson K, MacArthur DG, MacDonald JR, Onyiah I, Pang AW, Robson S, Stirrups K, Valsesia A, Walter K, Wei J, Wellcome Trust Case Control Consortium, Tyler-Smith C, Carter NP, Lee C, Scherer SW, Hurles ME (2010) Common copy number variation in the human genome: mechanism, selection and disease association. Nature 464(7289):704–712

    Article  CAS  PubMed  Google Scholar 

  • Di Fiore A, Rendell D (1994) Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc Natl Acad Sci USA 91:9941–9945

    Article  CAS  PubMed  Google Scholar 

  • Don RH, Cox PT, Wainwright BJ, Baker K, Mattick JS (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucl Acids Res 19(14):4008

    Article  CAS  PubMed  Google Scholar 

  • Donaldson ZR, Kondrashov FA, Putnam A, Bai Y, Stoinski TL, Hammock EA, Young LJ (2008) Evolution of a behavior-linked microsatellite-containing element in the 5′ flanking region of the primate AVPR1A gene. BMC Evol Biol 23(8):180

    Article  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed  Google Scholar 

  • Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320

    CAS  PubMed  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    Article  PubMed  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinfor 1:e47–e50

    Google Scholar 

  • Felsenstein J (2005) PHYLIP (phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle (USA). http://evolution.genetics.washington.edu/phylip.html

  • Fernandez-Duque E (2009) Natal dispersal in monogamous owl monkeys (Aotus azarai) of the Argentinean Chaco. Behaviour 146:583–606

    Article  Google Scholar 

  • Fernandez-Duque E, Rotundo M (2003) Field methods for capturing and marking Araza’s night monkeys. Int J Primat 24:1113–1120

    Article  Google Scholar 

  • FigTrees v1.2.3 (2009) (A. Rambaut, http://beast.bio.ed.ac.uk/FigTree)

  • Fink S, Excoffier L, Heckel G (2006) Mammalian monogamy is not controlled by a single gene. Proc Natl Acad Sci USA 103(29):10956–10960

    Article  CAS  PubMed  Google Scholar 

  • Fink S, Excoffier L, Heckel G (2007) High variability and non-neutral evolution of the mammalian avpr1a gene. BMC Evol Biol 7:176

    Article  PubMed  Google Scholar 

  • Forster P, Harding R, Torroni A, Bandelt HJ (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet 59:935–945

    CAS  PubMed  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  Google Scholar 

  • Gökçümen Ö, Lee C (2009) Copy number variants (CNVs) in primate species using array-based comparative genomic hybridization. Methods 49(1):18–25

    Article  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hammock EA, Young LJ (2002) Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour. Eur J Neurosci 16(3):399–402

    Article  PubMed  Google Scholar 

  • Hammock EA, Young LJ (2004) Functional microsatellite polymorphism associated with divergent social structure in vole species. Mol Biol Evol 21(6):1057–1063

    Article  CAS  PubMed  Google Scholar 

  • Hammock EA, Young LJ (2005) Microsatellite instability generates diversity in brain and sociobehavioral traits. Science 308(5728):1630–1634

    Article  CAS  PubMed  Google Scholar 

  • Hammock EA, Lim MM, Nair HP, Young LJ (2005) Association of vasopressin 1a receptor levels with a regulatory microsatellite and behavior. Genes Brain Behav 4(5):289–301

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568

    Article  CAS  PubMed  Google Scholar 

  • Hodgson JA, Sterner KN, Matthews LJ, Burrell AS, Jani RA, Raaum RL, Stewart CB, Disotell TR (2009) Successive radiations, not stasis, in the South American primate fauna. Proc Natl Acad Sci USA 106(14):5534–5539

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294(5550):2310–2314

    Article  CAS  PubMed  Google Scholar 

  • Iafrate AJ, Feuk L, Rivera MN, Listewnik ML, Donahoe PK, Qi Y, Scherer SW, Lee C (2004) Detection of large-scale variation in the human genome. Nat Genet 36(9):949–951

    Article  CAS  PubMed  Google Scholar 

  • Insel TR (2003) Is social attachment an addictive disorder? Physiol Behav 79(3):351–357

    Article  CAS  PubMed  Google Scholar 

  • Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, Diekhans M, Giardine B, Harte RA, Hinrichs AS, Hsu F, Miller W, Pedersen JS, Pohl A, Raney BJ, Rhead B, Rosenbloom KR, Smith KE, Stanke M, Thakkapallayil A, Trumbower H, Wang T, Zweig AS, Haussler D, Kent WJ (2008) The UCSC genome browser database: 2008 update. Nucl Acids Res 36:773–779

    Article  Google Scholar 

  • Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12(6):996–1006

    CAS  PubMed  Google Scholar 

  • Kim SJ, Young LJ, Gonen D, Veenstra-VanderWeele J, Courchesne R, Courchesne E, Lord C, Leventhal BL, Cook EH Jr, Insel TR (2002) Transmission disequilibrium testing of arginine vasopressin receptor 1A (AVPR1A) polymorphisms in autism. Mol Psychiatry 7(5):503–507

    Article  CAS  PubMed  Google Scholar 

  • Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69

    Article  CAS  PubMed  Google Scholar 

  • Korbie DJ, Mattick JS (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat Protoc 3(9):1452–1456

    Article  CAS  PubMed  Google Scholar 

  • Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R, Siepel A (2008) Patterns of positive selection in six mammalian genomes. PLoS Genet 4(8):e1000144

    Article  PubMed  Google Scholar 

  • Lim MM, Hammock EA, Young LJ (2004a) The role of vasopressin in the genetic and neural regulation of monogamy. Neuroendocrin 16(4):325–332

    Article  CAS  Google Scholar 

  • Lim MM, Wang Z, Olazábal DE, Ren X, Terwilliger EF, Young LJ (2004b) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429(6993):754–757

    Article  CAS  PubMed  Google Scholar 

  • Maddison DR, Maddison WP (2003) MacClade 4: analysis of phylogeny and character evolution, Version 4.06. Sinauer and Associates, Sunderland, MA

    Google Scholar 

  • Mendoza SP, Reeder DM, Mason WA (2002) Nature of proximate mechanisms underlying primate social systems: simplicity and redundancy. Evol Anthropol 11(S1):112–116

    Article  Google Scholar 

  • Mock DW, Fujioka M (1990) Monogamy and long-term pair bonding in vertebrates. Trends Ecol Evol 5(2):39–43

    Article  Google Scholar 

  • Moller AP (2003) The evolution of monogamy: mating relationships, parental care and sexual selection. In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. University of Cambridge Press, Cambridge, pp 29–41

    Google Scholar 

  • Murasawa S, Matsubara H, Kijima K, Maruyama K, Mori Y, Inada M (1995) Structure of the rat V1a vasopressin receptor gene and characterization of its promoter region and complete cDNA sequence of the 3’-end. J Biol Chem 270(34):20042–20050

    Article  CAS  PubMed  Google Scholar 

  • Opazo JC, Wildman DE, Prychitko T, Johnson RM, Goodman M (2006) Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates). Mol Phylogenet Evol 40(1):274–280

    Article  CAS  PubMed  Google Scholar 

  • Palombit RA (1994) Dynamic pair bonds in hylobatids: implications regarding monogamous social systems. Behaviour 128:65–101

    Article  Google Scholar 

  • Park H, Kim JI, Ju YS, Gokcumen O, Mills RE, Kim S, Lee S, Suh D, Hong D, Kang HP, Yoo YJ, Shin JY, Kim HJ, Yavartanoo M, Chang YW, Ha JS, Chong W, Hwang GR, Darvishi K, Kim H, Yang SJ, Yang KS, Kim H, Hurles ME, Scherer SW, Carter NP, Tyler-Smith C, Lee C, Seo JS (2010) Discovery of common Asian copy number variants using integrated high-resolution array CGH and massively parallel DNA sequencing. Nat Genet 42(5):400–405

    Article  CAS  PubMed  Google Scholar 

  • Phelps SM, Campbell P, Zheng DJ, Ophir AG (2009) Beating the boojum: comparative approaches to the neurobiology of social behavior. Neuropharma 58(1):17–28

    Article  Google Scholar 

  • Pitkow LJ, Sharer CA, Ren X, Insel TR, Terwilliger EF, Young LJ (2001) Facilitation of affiliation and pair-bond formation by vasopressin receptor gene transfer into the ventral forebrain of a monogamous vole. J Neurosci 21(18):7392–7396

    CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Poux C, Chevret P, Huchon D, De Jong WW, Douzery EJP (2006) Arrival and diversification of caviomorph rodents and platyrrhine primates in South America. Syst Biol 55(2):228–244

    Article  PubMed  Google Scholar 

  • Rambaut A, Drummond AJ (2007) Tracer v1.5. http://beast.bio.ed.ac.uk/Tracer

  • Rendell D, Di Fiore A (2007) Homoplasy, homology, and the perceived special status of behavior in evolution. J Hum Evol 52:504–521

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3, Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rosso L, Keller L, Kaessmann H, Hammond RL (2008) Mating system and avpr1a promoter variation in primates. Biol Lett 4(4):375–378

    Article  PubMed  Google Scholar 

  • Rotundo M, Fernandez-Duque E, Dixson A (2005) Infant development and parental care in free-ranging Aotus azarai azarai in Argentina. Int J Primat 26:1459–1473

    Article  Google Scholar 

  • Rozas J, Sanchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP: DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*, phylogenetic analysis using parsimony (and other methods), Version 4.0b10 Beta. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  Google Scholar 

  • Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genetics 123:597–601

    CAS  PubMed  Google Scholar 

  • Tejedor MF, Tauber AA, Rosenberger AL, Swisher CC, Palacios ME (2006) New primate genus from the Miocene of Argentina. Proc Natl Acad Sci USA 103(14):5437–5441

    Article  CAS  PubMed  Google Scholar 

  • Thibonnier M, Graves MK, Wagner MS, Auzan C, Clauser E, Willard HF (1996) Structure, sequence, expression and chromosomal location of the human V1a vasopressin receptor gene. Genomics 31:327–334

    Article  CAS  PubMed  Google Scholar 

  • Thibonnier M, Graves MK, Wagner MS, Chatelain N, Soubrier F, Corvol P, Willard HF, Jeunemaitre X (2000) Study of V(1)-vascular vasopressin receptor gene microsatellite polymorphisms in human essential hypertension. J Mol Cell Cardiol 32:557–564

    Article  CAS  PubMed  Google Scholar 

  • Turner LM, Young AR, Rompler H, Schoneberg T, Phelps SM, Hoekstra HE (2010) Monogamy evolves through multiple mechanisms: evidence from V1aR in deer mice. Mol Biol Evol 27(6):1269–1278

    Article  CAS  PubMed  Google Scholar 

  • Van Schaik CP, Dunbar RIM (1990) The evolution of monogamy in large primates: a new hypothesis and some crucial tests. Behaviour 115(1–2):30–61

    Article  Google Scholar 

  • Van Schaik CP, Kappeler PM (2003) The evolution of social monogamy in primates. In: Reichard UH, Boesch C (eds) Monogamy: mating strategies and partnerships in birds, humans and other mammals. University of Cambridge Press, Cambridge, pp 59–80

    Google Scholar 

  • Van Schaik CP, Van Hoof JARAM (1983) On the ultimate causes of primate social systems. Behaviour 85(1–2):91–117

    Article  Google Scholar 

  • Walum H, Westberg L, Henningsson S, Neiderhiser JM, Reiss D, Igl W, Ganiban JM, Spotts EL, Pedersen NL, Eriksson E, Lichtenstein P (2008) Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc Natl Acad Sci USA 105(37):14153–14156

    Article  CAS  PubMed  Google Scholar 

  • Wildman DE, Jameson NM, Opazon JC, Yi SV (2009) A fully resolved genus level phylogeny of neotropical primates (Platyrrhini). Mol Phy Evol 53(3):694–702

    Article  CAS  Google Scholar 

  • Wright PC (1994) The behavior and ecology of the owl monkey. In: Baer JF, Weller RE, Kakoma I (eds) Aotus: the owl monkey. Academic Press, San Diego, CA, pp 97–113

    Google Scholar 

  • Yang Z (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591

    Article  CAS  PubMed  Google Scholar 

  • Young LJ, Hammock EA (2007) On switches and knobs, microsatellites and monogamy. Trends Genet 23(5):209–212

    Article  CAS  PubMed  Google Scholar 

  • Young LJ, Nilsen R, Waymire KG, MacGregor GR, Insel TR (1999) Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400:766–768

    Article  CAS  PubMed  Google Scholar 

  • Young LJ, Murphy Young AZ, Hammock EA (2005) Anatomy and neurochemistry of the pair bond. J Comp Neurol 493(1):51–57

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Dr. Ömer Gökçümen for his assistance with statistical calculations, Dr. Richard Smith for advice with transcription factor mapping, and two anonymous reviewers whose comments on earlier versions of this manuscript were invaluable. This study was supported by a University Research Fund award from the University of Pennsylvania (EFD), and research funds from the Department of Anthropology at the University of Pennsylvania (PLB). E.F.D. also acknowledges continuing financial support from the Wenner-Gren Foundation, the L.S.B. Leakey Foundation, the National Geographic Society, the National Science Foundation (BCS-0621020), and the Zoological Society of San Diego. T.G.S. further acknowledges the infrastructural support provided by the National Geographic Society.

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Babb, P.L., Fernandez-Duque, E. & Schurr, T.G. AVPR1A Sequence Variation in Monogamous Owl Monkeys (Aotus azarai) and Its Implications for the Evolution of Platyrrhine Social Behavior. J Mol Evol 71, 279–297 (2010). https://doi.org/10.1007/s00239-010-9383-6

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