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02 12, 2021;11 (1): 3746.

Neural correlates of mating system diversity: oxytocin and vasopressin receptor distributions in monogamous and non-monogamous Eulemur.

Nicholas M Grebe, Annika Sharma, Sara M Freeman, Michelle C Palumbo, Heather B Patisaul, Karen L Bales, Christine M Drea
Author Information
  1. Nicholas M Grebe: Department of Evolutionary Anthropology, Duke University, Durham, NC, USA. nicholas.grebe@duke.edu.
  2. Annika Sharma: Department of Evolutionary Anthropology, Duke University, Durham, NC, USA.
  3. Sara M Freeman: Department of Psychology, California National Primate Research Center, University of California-Davis, Davis, CA, USA.
  4. Michelle C Palumbo: Department of Psychology, California National Primate Research Center, University of California-Davis, Davis, CA, USA.
  5. Heather B Patisaul: Department of Biological Sciences, North Carolina State University, Raleigh, NC, USA.
  6. Karen L Bales: Department of Psychology, California National Primate Research Center, University of California-Davis, Davis, CA, USA.
  7. Christine M Drea: Department of Evolutionary Anthropology, Duke University, Durham, NC, USA.
PMID: 33580133 DOI: 10.1038/s41598-021-83342-6

Abstract

Contemporary theory that emphasizes the roles of oxytocin and vasopressin in mammalian sociality has been shaped by seminal vole research that revealed interspecific variation in neuroendocrine circuitry by mating system. However, substantial challenges exist in interpreting and translating these rodent findings to other mammalian groups, including humans, making research on nonhuman primates crucial. Both monogamous and non-monogamous species exist within Eulemur, a genus of strepsirrhine primate, offering a rare opportunity to broaden a comparative perspective on oxytocin and vasopressin neurocircuitry with increased evolutionary relevance to humans. We performed oxytocin and arginine vasopressin 1a receptor autoradiography on 12 Eulemur brains from seven closely related species to (1) characterize receptor distributions across the genus, and (2) examine differences between monogamous and non-monogamous species in regions part of putative "pair-bonding circuits". We find some binding patterns across Eulemur reminiscent of olfactory-guided rodents, but others congruent with more visually oriented anthropoids, consistent with lemurs occupying an 'intermediary' evolutionary niche between haplorhine primates and other mammalian groups. We find little evidence of a "pair-bonding circuit" in Eulemur akin to those proposed in previous rodent or primate research. Mapping neuropeptide receptors in these nontraditional species questions existing assumptions and informs proposed evolutionary explanations about the biological bases of monogamy.

References

  1. Goodson, J. L. The vertebrate social behavior network: evolutionary themes and variations. Horm. Behav. 48(1), 11–22 (2005). [PMID: 15885690]
  2. Carter, C. S. Oxytocin and sexual behavior. Neurosci. Biobehav. Rev. 16(2), 131–144 (1992). [PMID: 1630727]
  3. Cho, M. M., DeVries, A. C., Williams, J. R. & Carter, C. S. The effects of oxytocin and vasopressin on partner preferences in male and female prairie voles (Microtus ochrogaster). Behav. Neurosci. 113(5), 1071–1079 (1999). [PMID: 10571489]
  4. Young, L. J. & Wang, Z. The neurobiology of pair bonding. Nat. Neurosci. 7(10), 1048–1054 (2004). [PMID: 15452576]
  5. Borrow, A. P. & Cameron, N. M. The role of oxytocin in mating and pregnancy. Horm. Behav. 61(3), 266–276 (2012). [PMID: 22107910]
  6. Wang, Z., Young, L. J., De Vries, G. J. & Insel, T. R. Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog. Brain Res. 119, 483–499 (1998). [PMID: 10074808]
  7. Feldman, R. Oxytocin and social affiliation in humans. Horm. Behav. 61(3), 380–391 (2012). [PMID: 22285934]
  8. Neumann, I. D. & Landgraf, R. Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors. Trends Neurosci. 35(11), 649–659 (2012). [PMID: 22974560]
  9. Cavanaugh, J., Carp, S. B., Rock, C. M. & French, J. A. Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys. Psychoneuroendocrinology. 66, 22–30 (2016). [PMID: 26771946]
  10. Potegal, M. & Ferris, C. F. Intraspecific aggression in male hamsters is inhibited by intrahypothalamic vasopressin-receptor antagonist. Aggress. Behav. 15(4), 311–320 (1989). [DOI: 10.1002/ab.2480150406]
  11. De Dreu, C. K. W. et al. The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328(5984), 1408–1411 (2010). [PMID: 20538951]
  12. Dölen, G., Darvishzadeh, A., Huang, K. W. & Malenka, R. C. Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501(7466), 179–184 (2013). [PMID: 24025838]
  13. Ferguson, J. N., Aldag, J. M., Insel, T. R. & Young, L. J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21(20), 8278–8285 (2001). [PMID: 11588199]
  14. Lopatina, O. L., Komleva, Y. K., Gorina, Y. V., Higashida, H. & Salmina, A. B. Neurobiological aspects of face recognition: the role of oxytocin. Front. Behav. Neurosci. 12, 195 (2018). [PMID: 30210321]
  15. Freeman, S. M. & Bales, K. L. Oxytocin, vasopressin, and primate behavior: diversity and insight. Am. J. Primatol. 80(10), e22919 (2018). [PMID: 30281814]
  16. Putnam, P. T., Young, L. J. & Gothard, K. M. Bridging the gap between rodents and humans: the role of non-human primates in oxytocin research. Am. J. Primatol. 80(10), e22756 (2018). [PMID: 29923206]
  17. Caldwell, H. K., & Young, W. S. Oxytocin and vasopressin: genetics and behavioral implications. In Handbook of Neurochemistry and Molecular Neurobiology 573–607 (Boston, MA, Springer US, 2006).
  18. Insel, T. R. & Shapiro, L. E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. USA 89(13), 5981–5985 (1992). [PMID: 1321430]
  19. Insel, T. R., Wang, Z. X. & Ferris, C. F. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents. J. Neurosci. 14(9), 5381–5392 (1994). [PMID: 8083743]
  20. Lim, M. M., Murphy, A. Z. & Young, L. J. Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster). J. Comp. Neurol. 468(4), 555–570 (2004). [PMID: 14689486]
  21. Smeltzer, M. D., Curtis, J. T., Aragona, B. J. & Wang, Z. Dopamine, oxytocin, and vasopressin receptor binding in the medial prefrontal cortex of monogamous and promiscuous voles. Neurosci. Lett. 394(2), 146–151 (2006). [PMID: 16289323]
  22. Beery, A. K., Lacey, E. A. & Francis, D. D. Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco-tuco (Ctenomys haigi and Ctenomys sociabilis). J. Comp. Neurol. 507(6), 1847–1859 (2008). [PMID: 18271022]
  23. Campbell, P., Ophir, A. G. & Phelps, S. M. Central vasopressin and oxytocin receptor distributions in two species of singing mice. J. Comp. Neurol. 516(4), 321–333 (2009). [PMID: 19637308]
  24. Carter, C. S., DeVries, A. C. & Getz, L. L. Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci. Biobehav. Rev. 19(2), 303–314 (1995). [PMID: 7630584]
  25. Insel, T. R. The challenge of translation in social neuroscience: A review of oxytocin, vasopressin, and affiliative behavior. Neuron 65(6), 768–779 (2010). [PMID: 20346754]
  26. Madrid, J. E., Parker, K. J., & Ophir, A. G. Variation, plasticity, and alternative mating tactics: Revisiting what we know about the socially monogamous prairie vole. In Advances in the Study of Behavior 203–42 (Elsevier, 2020).
  27. Phelps, S. M. & Young, L. J. Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): patterns of variation and covariation. J. Comp. Neurol. 466(4), 564–576 (2003). [PMID: 14566950]
  28. King, L. B., Walum, H., Inoue, K., Eyrich, N. W. & Young, L. J. Variation in the oxytocin receptor gene predicts brain region–specific expression and social attachment. Biol. Psychiatry. 80(2), 160–169 (2016). [PMID: 26893121]
  29. Walum, H. & Young, L. J. The neural mechanisms and circuitry of the pair bond. Nat. Rev. Neurosci. 19(11), 643–654 (2018). [PMID: 30301953]
  30. Beach, F. A. The Snark was a Boojum. Am. Psychol. 5(4), 115–124 (1950). [DOI: 10.1037/h0056510]
  31. Preuss, T. M. Taking the measure of diversity: comparative alternatives to the model-animal paradigm in cortical neuroscience. Brain Behav. Evol. 55(6), 287–299 (2000). [PMID: 10971014]
  32. Thompson, R. R. An updated field guide for snark hunting: Comparative contributions to behavioral neuroendocrinology in the era of model organisms. Horm. Behav. 122(104742), 104742 (2020). [PMID: 32173444]
  33. Boldog, E. et al. Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type. Nat. Neurosci. 21(9), 1185–1195 (2018). [PMID: 30150662]
  34. Hodge, R. D. et al. Conserved cell types with divergent features in human versus mouse cortex. Nature 573(7772), 61–68 (2019). [PMID: 31435019]
  35. Fleagle, J. G. Primate Adaptation and Evolution 3rd edn. (CA, Academic Press, San Diego, 2013).
  36. Hozer, C., Pifferi, F., Aujard, F. & Perret, M. The biological clock in gray mouse lemur: Adaptive, evolutionary and aging considerations in an emerging non-human primate model. Front Physiol. 10, 1033 (2019). [PMID: 31447706]
  37. Ezran, C. et al. The mouse lemur, a genetic model organism for primate biology, behavior, and health. Genetics 206(2), 651–664 (2017). [PMID: 28592502]
  38. Ossi, K. & Kamilar, J. M. Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav. Ecol. Sociobiol. 61(1), 53–64 (2006). [DOI: 10.1007/s00265-006-0236-7]
  39. Kappeler, P. M. & Fichtel, C. The evolution of Eulemur social organization. Int. J. Primatol. 37(1), 10–28 (2016). [DOI: 10.1007/s10764-015-9873-x]
  40. Tecot, S. R., Singletary, B. & Eadie, E. Why, “monogamy” isn’t good enough: pair-living, pair-bonding, and monogamy. Am. J. Primatol. 78(3), 340–354 (2016). [PMID: 25864507]
  41. Lukas, D. & Clutton-Brock, T. H. The evolution of social monogamy in mammals. Science 341(6145), 526–530 (2013). [PMID: 23896459]
  42. Singletary, B. & Tecot, S. Signaling across the senses: a captive case study in pair-bonded red-bellied lemurs (Eulemur rubriventer) at the Duke Lemur Center, NC. USA. Primates. 60(6), 499–505 (2019). [PMID: 31650280]
  43. Shultz, S., Opie, C. & Atkinson, Q. D. Stepwise evolution of stable sociality in primates. Nature 479(7372), 219–222 (2011). [PMID: 22071768]
  44. Tobin, V. A. et al. An intrinsic vasopressin system in the olfactory bulb is involved in social recognition. Nature 464(7287), 413–417 (2010). [PMID: 20182426]
  45. Freeman SM, Young LJ. Comparative perspectives on oxytocin and vasopressin receptor research in rodents and primates: translational implications. J. Neuroendocrinol. 2016;28(4).
  46. Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M. & Young, L. J. The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta). Psychoneuroendocrinology. 45, 128–141 (2014). [PMID: 24845184]
  47. Freeman, S. M. et al. Neuroanatomical distribution of oxytocin and vasopressin 1a receptors in the socially monogamous coppery titi monkey (Callicebus cupreus). Neuroscience 273, 12–23 (2014). [PMID: 24814726]
  48. Freeman, S. M., Smith, A. L., Goodman, M. M. & Bales, K. L. Selective localization of oxytocin receptors and vasopressin 1a receptors in the human brainstem. Soc. Neurosci. 12(2), 113–123 (2017). [PMID: 26911439]
  49. Bales, K. L. et al. Titi monkeys as a novel non-human primate model for the neurobiology of pair bonding. Yale J. Biol. Med. 90(3), 373–387 (2017). [PMID: 28955178]
  50. The IUCN Red List of Threatened Species. 2020–2 [cited 2020 Jul 9]. Available from: https://www.iucnredlist.org
  51. Markolf, M. & Kappeler, P. M. Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar. Front Zool. 10(1), 70 (2013). [PMID: 24228694]
  52. Freeman, S. M. et al. Effect of age and autism spectrum disorder on oxytocin receptor density in the human basal forebrain and midbrain. Transl. Psychiatry. 8(1), 257 (2018). [PMID: 30514927]
  53. Smith, A. L. et al. Initial investigation of three selective and potent small molecule oxytocin receptor PET ligands in New World monkeys. Bioorg. Med. Chem. Lett. 26(14), 3370–3375 (2016). [PMID: 27209233]
  54. Bakker, R., Tiesinga, P. & Kötter, R. The Scalable Brain Atlas: Instant web-based access to public brain atlases and related content. Neuroinformatics. 13(3), 353–366 (2015). [PMID: 25682754]
  55. Rohlfing, T. et al. The INIA19 template and NeuroMaps atlas for primate brain image parcellation and spatial normalization. Front. Neuroinform. 6, 27 (2012). [PMID: 23230398]
  56. Ding, S.-L., Royall, J. J., Sunkin, S. M., Ng, L., Facer, B. A. C., Lesnar, P. et al. Comprehensive cellular-resolution atlas of the adult human brain: adult human brain atlas. J. Comp. Neurol. 524(16), Spc1–Spc1 (2016).
  57. Schorscher-Petcu, A., Dupré, A. & Tribollet, E. Distribution of vasopressin and oxytocin binding sites in the brain and upper spinal cord of the common marmoset. Neurosci. Lett. 461(3), 217–222 (2009). [PMID: 19539696]
  58. Wacker, D. & Ludwig, M. The role of vasopressin in olfactory and visual processing. Cell Tissue Res. 375(1), 201–215 (2019). [PMID: 29951699]
  59. Heritage, S. Modeling olfactory bulb evolution through primate phylogeny. PLoS ONE 9(11), e113904 (2014). [PMID: 25426851]
  60. Drea, C. M. D’scent of man: a comparative survey of primate chemosignaling in relation to sex. Horm. Behav. 68, 117–133 (2015). [PMID: 25118943]
  61. Drea, C. M. Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2020(375), 20190264 (1800).
  62. Lazaro-Perea, C., Snowdon, C. T. & de Fátima, A. M. Scent-marking behavior in wild groups of common marmosets (Callithrix jacchus). Behav. Ecol. Sociobiol. 46(5), 313–324 (1999). [DOI: 10.1007/s002650050625]
  63. Changizi, M. A., Zhang, Q. & Shimojo, S. Bare skin, blood and the evolution of primate colour vision. Biol. Lett. 2(2), 217–221 (2006). [PMID: 17148366]
  64. Fernandez, A. A. & Morris, M. R. Sexual selection and trichromatic color vision in primates: statistical support for the preexisting-bias hypothesis. Am. Nat. 170(1), 10–20 (2007). [PMID: 17853988]
  65. Emery, N. J. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci. Biobehav. Rev. 24(6), 581–604 (2000). [PMID: 10940436]
  66. Shepherd, S. V. & Platt, M. L. Spontaneous social orienting and gaze following in ringtailed lemurs (Lemur catta). Anim. Cogn. 11(1), 13–20 (2008). [PMID: 17492318]
  67. Freeman, A. R., Aulino, E. A., Caldwell, H. K. & Ophir, A. G. Comparison of the distribution of oxytocin and vasopressin 1a receptors in rodents reveals conserved and derived patterns of nonapeptide evolution. J. Neuroendocrinol. 32(4), e12828 (2020). [PMID: 31925983]
  68. Baxter, A. et al. Oxytocin receptor binding in the titi monkey hippocampal formation is associated with parental status and partner affiliation. Sci. Rep. 10(1), 1–14 (2020). [DOI: 10.1038/s41598-020-74243-1]
  69. Cilz, N. I., Cymerblit-Sabba, A. & Young, W. S. Oxytocin and vasopressin in the rodent hippocampus. Genes Brain Behav. 18(1), e12535 (2019). [PMID: 30378258]
  70. Pagani, J. H. et al. Role of the vasopressin 1b receptor in rodent aggressive behavior and synaptic plasticity in hippocampal area CA2. Mol. Psychiatry. 20(4), 490–499 (2015). [PMID: 24863146]
  71. Jankowski, M. M. et al. The anterior thalamus provides a subcortical circuit supporting memory and spatial navigation. Front. Syst. Neurosci. 7, 45 (2013). [PMID: 24009563]
  72. Nakamura, K. The role of the dorsal raphé nucleus in reward-seeking behavior. Front. Integr. Neurosci. 7, 60 (2013). [PMID: 23986662]
  73. Rood, B. D. & Beck, S. G. Vasopressin indirectly excites dorsal raphe serotonin neurons through activation of the vasopressin1A receptor. Neuroscience 260, 205–216 (2014). [PMID: 24345477]
  74. Mierop, A. et al. How can intranasal oxytocin research be trusted? A systematic review of the interactive effects of intranasal oxytocin on psychosocial outcomes. Perspect. Psychol. Sci. 15(5), 1228–1242 (2020). [PMID: 32633663]
  75. Rosenthal, M. F., Gertler, M., Hamilton, A. D., Prasad, S. & Andrade, M. C. B. Taxonomic bias in animal behavior publications. Anim. Behav. 127, 83–89 (2017). [DOI: 10.1016/j.anbehav.2017.02.017]
  76. Huck, M., Di Fiore, A. & Fernandez-Duque, E. Of apples and oranges? The evolution of “monogamy” in non-human primates. Front. Ecol. Evol. 7, 472 (2020). [DOI: 10.3389/fevo.2019.00472]

Grants

  1. P30 ES025128/NIEHS NIH HHS
  2. R21 MH115680/NIMH NIH HHS

MeSH Term

Animals
Biological Evolution
Brain
Brain Mapping
Evolution, Molecular
Female
Lemuridae
Male
Memory
Neurosecretory Systems
Oxytocin
Pair Bond
Primates
Receptors, Oxytocin
Receptors, Vasopressin
Reproduction
Sexual Behavior, Animal
Social Behavior
Species Specificity
Vasopressins

Chemicals

Receptors, Oxytocin
Receptors, Vasopressin
Vasopressins
Oxytocin
Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't
Article has an altmetric score of 208

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