Oxytocin receptor gene sequences in owl monkeys and other primates show remarkable interspecific regulatory and protein coding variation
Open accessAbstract
The oxytocin (OT) hormone pathway is involved in numerous physiological processes, and one of its receptor genes (OXTR) has been implicated in pair bonding behavior in mammalian lineages. This observation is important for understanding social monogamy in primates, which occurs in only a small subset of taxa, including Azara's owl monkey (Aotus azarae). To examine the potential relationship between social monogamy and OXTR variation, we sequenced its 5' regulatory (4936bp) and coding (1167bp) regions in 25 owl monkeys from the Argentinean Gran Chaco, and examined OXTR sequences from 1092 humans from the 1000 Genomes Project. We also assessed interspecific variation of OXTR in 25 primate and rodent species that represent a set of phylogenetically and behaviorally disparate taxa. Our analysis revealed substantial variation in the putative 5' regulatory region of OXTR, with marked structural differences across primate taxa, particularly for humans and chimpanzees, which exhibited unique patterns of large motifs of dinucleotide A+T repeats upstream of the OXTR 5' UTR. In addition, we observed a large number of amino acid substitutions in the OXTR CDS region among New World primate taxa that distinguish them from Old World primates. Furthermore, primate taxa traditionally defined as socially monogamous (e.g., gibbons, owl monkeys, titi monkeys, and saki monkeys) all exhibited different amino acid motifs for their respective OXTR protein coding sequences. These findings support the notion that monogamy has evolved independently in Old World and New World primates, and that it has done so through different molecular mechanisms, not exclusively through the oxytocin pathway.
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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).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [109]
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 [109]
Monogamy has evolved independently in Great Apes and New World monkeys by potentially different molecular mechanisms.
“This finding suggests that monogamy has evolved independently in Great Apes and NWMs by potentially different molecular mechanisms (Babb et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Babb et al., 2015
An independent survey demonstrated important differences in amino acid motifs in OT coding regions across socially monogamous primates.
“Another independent survey of the OTR variability in primates demonstrated important differences in amino acid motifs in OT coding regions across socially monogamous primates (e.g., humans, gibbons, owl monkeys, titi monkeys, saki monkeys; Babb et al., 2015).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Babb 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 Babb, Fernandez-Duque, & Schurr, 2015
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Vargas-Pinilla, P., Paixão-Côrtes, V. R., Paré, P., Tovo-Rodrigues, L., Vieira, C. M. D. A. G., Xavier, A., Comas, D., Pissinatti, A., Sinigaglia, M., Rigo, M. M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419399112 · Cited by 59 · see citing works
Association between the oxytocin receptor (OXTR) gene and mesolimbic responses to rewards
Damiano, C. R., Aloi, J. M., Dunlap, K., Burrus, C. J., Mosner, M. G., Kozink, R. V., McLaurin, R. E., Mullette-Gillman, O. A., Carter, R., Huettel, S. A., et al. (2014) · Molecular Autism · doi:10.1186/2040-2392-5-7 · Cited by 54 · see citing works
Wartmann, F. M., Juárez, C. P., & Fernández‐Duque, E. (2014) · International Journal of Primatology · doi:10.1007/s10764-014-9771-7 · Cited by 48 · see citing works
Corticotropin-releasing hormone-binding protein in primates
Bowman, M. E., Lopata, A., Jaffe, R. B., Golos, T. G., Wickings, J., & Smith, R. (2001) · American Journal of Primatology · doi:10.1002/1098-2345(200103)53:3 · Cited by 46 · see citing works
Food transfers to young and mates in wild owl monkeys (Aotus azarai)
Wolovich, C. K., Perea-Rodríguez, J. P., & Fernández‐Duque, E. (2007) · American Journal of Primatology · doi:10.1002/ajp.20477 · Cited by 45 · see citing works
mtDNA diversity in azara's owl monkeys (Aotus azarai azarai) of the Argentinean Chaco
Babb, P. L., Fernández‐Duque, E., Baiduc, C. A., Gagneux, P., Evans, S., & Schurr, T. G. (2011) · American Journal of Physical Anthropology · doi:10.1002/ajpa.21567 · Cited by 43 · see citing works
Self-citationThe evolution of monogamy: mating relationships, parental care and sexual selection
Møller, A. P. (2003) · Cambridge University Press eBooks · doi:10.1017/cbo9781139087247.002 · Cited by 42 · see citing works
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When Dads Help: Male Behavioral Care During Primate Infant Development
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Regulatory element copy number differences shape primate expression profiles
Iskow, R. C., Gökçümen, Ö., Abyzov, A. S., Malukiewicz, J., Zhu, Q., Sukumar, A. T., Pai, A. A., Mills, R. E., Habegger, L., Cusanovich, D. A., et al. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205199109 · Cited by 40 · see citing works
Fernández‐Duque, E. (2015) · American Journal of Primatology · doi:10.1002/ajp.22397 · Cited by 39 · see citing works
Babb, P. L., Fernández‐Duque, E., & Schurr, T. G. (2010) · Journal of Molecular Evolution · doi:10.1007/s00239-010-9383-6 · Cited by 29 · see citing works
Self-citationNature of proximate mechanisms underlying primate social systems: Simplicity and redundancy
Mendoza, S. P., Reeder, D. M., & Mason, W. A. (2003) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/evan.10071 · Cited by 22 · see citing works
Alkemio: association of chemicals with biomedical topics by text and data mining
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Babb, P. L., McIntosh, A. M., Fernández‐Duque, E., Fiore, A. D., & Schurr, T. G. (2011) · Folia Primatologica · doi:10.1159/000330564 · Cited by 12 · see citing works
Self-citationBabb, P. L., McIntosh, A. M., Fernández‐Duque, E., & Schurr, T. G. (2013) · International Journal of Primatology · doi:10.1007/s10764-013-9721-9 · Cited by 6 · see citing works
Self-citationChini, B., Mouillac, B., ALA, Y., Balestre, M., Trumpp‐Kallmeyer, S., Hoflack, J., Elands, J., Hibert, M., Manning, M., Jard, S., et al. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb48181.x · Cited by 5 · see citing works
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Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“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).”
BackgroundNeuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
Mustoe, A. C., Harnisch, A. M., Hochfelder, B., Cavanaugh, J., & French, J. A. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.025 · Cited by 40 · see citing works
- Authors
- Babb, P. L., Fernandez-Duque, E., & Schurr, T. G.
- Affiliations
- University of Pennsylvania (US)
- Corresponding author
- Schurr, Theodore G.
- Venue
- Molecular Phylogenetics and Evolution
- Publisher
- Elsevier BV
- Published
- 2015-10
- Volume
- 91
- Pages
- 160-177
- ISSN
- 1055-7903 (ISSN-L)
- OpenAlex
- W406767003
- Cited by
- 16
- References
- 104
- Citations by year
- 2024: 3 · 2023: 1 · 2021: 2 · 2020: 1 · 2019: 1 · 2017: 2 · 2016: 5 · 2015: 1
- FWCI
- 4.37
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Phylogenetics and Evolution (acceptedVersion)
- PubMed (publishedVersion)
- Conicet (submittedVersion, cc-by-nc-sa)
- Funders
- GAPSA-Provost Award for Interdisciplinary Innovation
- L.S.B. Leakey Foundation (BCS-0621020)
- University Research Fund
- National Science Foundation
- National Geographic Society
- 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
- oxytocin receptor, owl monkey, Aotus azarae, social monogamy, pair bonding, 5' regulatory region, 5' untranslated region, amino acid substitutions, primate evolution, New World primates, Old World primates, titi monkeys, gibbons
- MeSH terms
- Animals, Humans, Mutation, Phylogeny, Primates, Proteins, Regulatory Sequences, Nucleic Acid, Genetic Variation, Aotidae, Sequence Analysis, DNA, Receptors, Oxytocin, Evolution, Molecular, Amino Acid Substitution, Mice, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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