Cited by 28Neuroendocrine regulation and behaviorPrimate Behavior and EcologyAnimal Behavior and Reproduction

Molecular Variation in AVP and AVPR1a in New World Monkeys (Primates, Platyrrhini): Evolution and Implications for Social Monogamy

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Ren, Dongren, Chin, Kelvin R., French, Jeffrey A.·2014·PLoS ONE

Abstract

The neurohypophysial hormone arginine vasopressin (AVP) plays important roles in fluid regulation and vascular resistance. Differences in AVP receptor expression, particularly mediated through variation in the noncoding promoter region of the primary receptor for AVP (AVPR1a), may play a role in social phenotypes, particularly social monogamy, in rodents and humans. Among primates, social monogamy is rare, but is common among New World monkeys (NWM). AVP is a nonapeptide and generally conserved among eutherian mammals, although a recent paper demonstrated that some NWM species possess a novel form of the related neuropeptide hormone, oxytocin. We therefore characterized variation in the AVP and AVPR1a genes in 22 species representing every genus in the three major platyrrhine families (Cebidae, Atelidae and Pitheciidae). For AVP, a total of 16 synonymous substitutions were detected in 15 NWM species. No non-synonymous substitutions were noted, hence, AVP is conserved in NWM. By contrast, relative to the human AVPR1a, 66 predicted amino acids (AA) substitutions were identified in NWM. The AVPR1a N-terminus (ligand binding domain), third intracellular (G-protein binding domain), and C-terminus were variable among species. Complex evolution of AVPR1a is also apparent in NWM. A molecular phylogenetic tree inferred from AVPR1a coding sequences revealed some consensus taxonomic separation by families, but also a mixed group composed of genera from all three families. The overall dN/dS ratio of AVPR1a was 0.11, but signals of positive selection in distinct AVPR1a regions were observed, including the N-terminus, in which we identified six potential positive selection sites. AA substitutions at positions 241, 319, 399 and 409 occurred uniquely in marmosets and tamarins. Our results enhance the appreciation of genetic diversity in the mammalian AVP/AVPR1a system, and set the stage for molecular modeling of the neurohypophyseal hormones and social behavior in primates.

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  • New World monkeys have genetic variation in OT and AVP peptide and receptor genes across species.

    “Species differences in receptor binding characteristics vary widely, especially in light of recent discoveries in New World monkeys, which show genetic variations in both the OT and AVP peptide and receptor genes across species (105-110).”
  • Receptor binding characteristics differ widely across species.

    “Species differences in receptor binding characteristics vary widely, especially in light of recent discoveries in New World monkeys, which show genetic variations in both the OT and AVP peptide and receptor genes across species (105-110).”
  • V1aR structure in New World monkeys differs significantly from receptors in other primate genera, especially in the N- and C-termini.

    “With regard to the AVP system, while there are no known variants in the AVP ligand in NWM, V1aR structure in NWM differs significantly from receptors in other primate genera especially in the N- and C-termini.”
  • Among New World monkeys there have been many physico-chemically radical and conservative amino acid substitutions in the N-terminus, third intracellular loop, and C-terminus when compared to the human V1aR.

    “Among NWM there have been many physico-chemically radical and conservative amino acid substitutions in the N-terminus, third intracellular loop, and C-terminus when compared to the human V1aR (Ren et al., 2014).”
  • A phylogeny generated using AVPR1a nucleotide sequences groups socially monogamous species more closely than grouping from canonical phylogenies.

    “Moreover, a phylogeny generated using AVPR1a nucleotide sequences groups socially monogamous species more closely than grouping from canonical phylogenies.”

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Authors
Ren, D., Chin, K. R., & French, J. A.
Affiliations
University of Nebraska at Omaha (US)
Corresponding author
Ren, Dongren
Venue
PLoS ONE
Published
2014-10-31
Volume
9
Issue
10
Pages
e111638
ISSN
1932-6203 (ISSN-L)
OpenAlex
W2133194321
Cited by
28
References
50
Citations by year
2026: 4 · 2025: 3 · 2024: 1 · 2021: 1 · 2020: 2 · 2019: 2 · 2018: 2 · 2017: 2 · 2016: 6 · 2015: 4 · 2014: 1
FWCI
6.43
Type
journal article
Language
en
Open access
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Institutes of Health (P51OD01107, RR013986, HD 042882, P51OD011107, P51OD011133)
  • National Center for Research Resources (RR-013986, P51RR013986)
  • California National Primate Research Center (HD071998, HD053555)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 042882, HD071998, R01HD042882, R01HD053555, R01HD071998, HD053555, R56HD042882)
  • Office of Research Infrastructure Programs, National Institutes of Health (P51 OD011133)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
Keywords
vasopressin, AVPR1A, arginine vasopressin receptor, New World monkeys, Platyrrhini, social monogamy, molecular evolution, positive selection, synonymous substitutions, nonsynonymous substitutions, oxytocin, marmoset, tamarins, ligand-binding domain, molecular phylogeny, dN/dS ratio, social behavior
MeSH terms
Animals, Arginine Vasopressin, Behavior, Animal, Biological Evolution, Humans, Models, Molecular, Molecular Sequence Data, Phylogeny, Social Behavior, Genetic Variation, Open Reading Frames, Receptors, Vasopressin, Platyrrhini

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