Genetic Diversity in Oxytocin Ligands and Receptors in New World Monkeys
Open accessAbstract
Oxytocin (OXT) is an important neurohypophyseal hormone that influences wide spectrum of reproductive and social processes. Eutherian mammals possess a highly conserved sequence of OXT (Cys-Tyr-Ile-Gln-Asn-Cys-Pro-Leu-Gly). However, in this study, we sequenced the coding region for OXT in 22 species covering all New World monkeys (NWM) genera and clades, and characterize five OXT variants, including consensus mammalian Leu(8)-OXT, major variant Pro(8)-OXT, and three previously unreported variants: Ala(8)-OXT, Thr(8)-OXT, and Phe(2)-OXT. Pro(8)-OXT shows clear structural and physicochemical differences from Leu(8)-OXT. We report multiple predicted amino acid substitutions in the G protein-coupled OXT receptor (OXTR), especially in the critical N-terminus, which is crucial for OXT recognition and binding. Genera with same Pro(8)-OXT tend to cluster together on a phylogenetic tree based on OXTR sequence, and we demonstrate significant coevolution between OXT and OXTR. NWM species are characterized by high incidence of social monogamy, and we document an association between OXTR phylogeny and social monogamy. Our results demonstrate remarkable genetic diversity in the NWM OXT/OXTR system, which can provide a foundation for molecular, pharmacological, and behavioral studies of the role of OXT signaling in regulating complex social phenotypes.
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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).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [105]
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).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [105]
Recent discoveries have identified surprising variability in OT and peptide structure in New World monkeys (NWM), with five new OT variants identified to date.
“recent discoveries have identified surprising variability in OT and peptide structure in New World monkeys (NWM), with five new OT variants identified to date”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Pithecidae displays three OT ligands, all varying at position 8 in the OT molecule (Leu8-, Thr8-, and Ala8-OT).
“Pithecidae displays three OT ligands, all varying at position 8 in the OT molecule (Leu8-, Thr8-, and Ala8-OT).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
The prevalence of nonsynonymous substitutions in OXT in every genus of New World monkeys codes for five distinct forms of OT in addition to consensus mammalian Leu8-OT, for a total of six OT ligand variants in this taxon.
“The feature that stands out most prominently is the prevalence of NSs in OXT in every genus of NWM, which in turn code for five distinct forms of OT in addition to consensus mammalian Leu8-OT, for a total of six OT ligand variants in this taxon.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
At least one genus in all three New World monkey families possesses a ligand variant.
“At least one genus in all three NWM families possesses a ligand variant.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
The OXT gene in all species other than New World monkeys codes for consensus mammalian Leu8-OT.
“First, the OXT gene in all species other than NWM codes for consensus mammalian, or Leu8-OT.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
In all ape and Old World primate species, OXT nucleotide sequences are identical to those in humans.
“In all ape and Old World primate species, OXT nucleotide sequences are identical to those in humans.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Atelidae displays three OT ligands (Leu8-, Pro8-, and Phe2-OT).
“Primates in the family Atelidae also display three OT ligands (Leu8-, Pro8-, and Phe2-OT).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Phe2-OT is the most hydrophobic variant, Leu8-OT is intermediate, while Pro8-OT is the most hydrophilic of the OT variants.
“For instance, Phe2-OT is the most hydrophobic variant, Leu8-OT is intermediate, while Pro8-OT is the most hydrophilic of the variants (Ren et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
None of the genera in the family Cebidae express Leu8-OT, but all genera have a nonsynonymous substitution in the 8th codon (CTG to CCG) leading to a proline residue in the 8th position.
“None of the genera in the family Cebidae express Leu8-OT, but all genera have a NS in the 8th codon (CTG → CCG) leading to a proline residue in the 8th position.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Ateles (family Atelidae) has an OTR structure more similar to genera in Cebidae than to its congeners Brachyteles and Lagothrix.
“Specifically, Ateles (family Atelidae), has an OTR structure that is more similar to the genera in Cebidae than to its congeners Brachyteles and Lagothrix.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Within New World monkeys, OTR sequence phylogenies significantly group by OT variants, social monogamy, and paternal care.
“examining OTR sequence phylogeny within the NWMs demonstrates OTR sequence phylogenies also significantly group by OT variants, social monogamy (Ren et al., 2015), and paternal care (Vargas-Pinilla et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Humans and Callithrix are more closely related to each other than to Otolemur, but Otolemur and human share the Leu8-OT.
“Humans and Callitrix are more closely related to each other than to Otolemur, but Otolemur and human share the Leu8-OT.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Some noteworthy deviations from the consensus New World monkey phylogenies can be identified.
“Importantly, some noteworthy deviations from the consensus NWM phylogenies (see Fig. 1) can be identified (Ren et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
The Callithrix OTR has more residue differences than the Otolemur OTR, particularly in the N-terminus critical for ligand recognition and binding.
“However, the Callithrix OTR has more residue differences than the Otolemur OTR, particularly in the N-terminus that has been shown to be critical for ligand recognition and binding.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
OTR variability among primates and especially New World monkeys has been significantly associated with social monogamy and paternal care in New World monkeys.
“OTR variability among primates and especially NWM has been significantly associated with the occurrence of two important social phenotypes in NWM: social monogamy (Ren et al., 2015) and paternal care in (Vargas-Pinilla et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
The association between OTR variability and sociality suggests that these systems are involved, at least in part, in the evolution and maintenance of these social phenotypes in New World monkeys.
“Overall, the association between OTR variability and sociality suggest that, at least in part, these systems are involved in the evolution and maintenance of these social phenotypes in NWM (Ren et al., 2015; Vargas-Pinilla et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Structural changes to the C-terminus tail of the Pro8-OT ligand might result in compensatory amino acid substitutions in the N-terminus of the receptor.
“It is reasonable that structural changes to the C-terminus tail of the Pro8-OT ligand might result in compensatory amino acid substitutions in the N-terminus of the receptor (Ren et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
Most residues critical for receptor binding or function are conserved in the OTR of New World monkey species.
“Most of the residues that have been shown or are predicted to be critical for receptor binding or function (reviewed in Gimpl and Fahrenholz, 2001; Koehbach et al., 2013) are conserved in the OTR of NWM species (Ren et al., 2015; Vargas-Pinilla et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
This residue may exhibit intraspecific polymorphism because one S. sciureus receptor sequence shows Phe115 and one shows Tyr115.
“This residue may also exhibit intraspecific polymorphism because one of the receptor sequences available for S. sciureus shows Phe115, and one shows Tyr115 (Lee et al., 2011; Ren et al., 2015; Vargas-Pinilla et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
OT ligand variation is statistically associated with the presence of social monogamy across NWM genera.
“While OT ligand variation has been statistically associated with the presence of social monogamy (Ren et al., 2015) and paternal care (Vargas-Pinilla et al., 2015) across NWM genera”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Ren et al., 2015
New World monkeys (NWMs), including callitrichids, possess notably remarkable interspecific OXT and OXT receptor (OXTR) diversity relative to other mammals.
“Second, New World monkeys (NWMs), including callitrichids, possess notably remarkable interspecific OXT and OXT receptor (OXTR) diversity relative to other mammals (Babb, Fernandez-Duque, & Schurr, 2015; Lee et al., 2011; Ren et al., 2015; Vargas-Pinilla et al., 2015; Wallis, 2012)”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Ren et al., 2015
These varied OXT/OXTR systems potentially coevolved to modulate species-specific social behaviour such as social monogamy and paternal care.
“and these varied OXT/OXTR systems potentially coevolved to modulate species-specific social behaviour such as social monogamy and paternal care (Ren et al., 2015; Vargas-Pinilla et al., 2015).”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Ren et al., 2015
The proline substitution results in a substantially altered structure in the "linear" portion of the molecule that likely affects OXT ligand-OXTR binding, and subsequently behavior.
“Due to a proline substitution at the 8th amino-acid position, the marmoset variant of OXT (Pro8-OXT) is distinctly different than the consensus mammalian variant of OXT (Leu8-OXT), and results in a substantially altered structure in the “linear” portion of the molecule that likely affects OXT ligand-OXTR binding, and subsequently behavior.”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Ren et al., 2015
Due to a proline substitution at the 8th amino-acid position, the marmoset variant of OXT (Pro8-OXT) is distinctly different than the consensus mammalian variant of OXT (Leu8-OXT).
“Due to a proline substitution at the 8th amino-acid position, the marmoset variant of OXT (Pro8-OXT) is distinctly different than the consensus mammalian variant of OXT (Leu8-OXT), and results in a substantially altered structure in the “linear” portion of the molecule that likely affects OXT ligand-OXTR binding, and subsequently behavior.”
From Marmosets treated with oxytocin are more socially attractive to their long-term mate (2015) · cites this paper as Ren et al., 2015
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- Authors
- Ren, D., Lu, G., Moriyama, H., Mustoe, A. C., Harrison, E. B., & French, J. A.
- Affiliations
- University of Nebraska at Omaha (US)
- University of Nebraska–Lincoln (US)
- Corresponding author
- Ren, Dongren
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2015-05-04
- Volume
- 10
- Issue
- 5
- Pages
- e0125775
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4418824
- OpenAlex
- W2113631199
- Cited by
- 47
- References
- 39
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 4 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 4 · 2019: 5 · 2018: 8 · 2017: 4 · 2016: 11 · 2015: 6
- FWCI
- 15.86
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DigitalCommons@UNO (submittedVersion, cc-by)
- Lincoln (University of Nebraska) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- University of Texas at Austin
- National Institutes of Health (P51OD01107, RR013986, HD 042882, 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, R01HD042882, R01HD053555, R01HD071998, 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 › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin, oxytocin receptor, New World monkeys, genetic diversity, G protein-coupled receptors, coevolution, social monogamy, primate phylogeny, social behavior
- MeSH terms
- Amino Acid Sequence, Animals, Behavior, Animal, Female, Male, Molecular Sequence Data, Oxytocin, Phylogeny, Genetic Variation, Sequence Alignment, Receptors, Oxytocin, Evolution, Molecular, Platyrrhini, Protein Interaction Domains and Motifs
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