Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy
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 soc...
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| description | 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. |
| doi_str_mv | 10.1371/journal.pone.0111638 |
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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.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0111638</identifier><identifier>PMID: 25360668</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acids ; Animals ; Arginine Vasopressin - genetics ; Argipressin ; Behavior, Animal ; Binding ; Biological Evolution ; Biology ; Biology and life sciences ; C-Terminus ; Coding ; Evolution ; Gene expression ; Genera ; Genetic diversity ; Genetic Variation ; Hormones ; Humans ; Kinases ; Ligands ; Mammals ; Microtus ; Models, Molecular ; Molecular modelling ; Molecular Sequence Data ; Monkeys ; Monogamy ; N-Terminus ; Neuropeptides ; Non-coding RNA ; Open Reading Frames - genetics ; Oxytocin ; Peromyscus ; Phylogeny ; Pituitary (posterior) ; Pituitary hormones ; Platyrrhini - genetics ; Positive selection ; Primates ; Protein binding ; Proteins ; Receptors, Vasopressin - genetics ; Rodentia ; Rodents ; Saimiri ; Signal transduction ; Social aspects ; Social Behavior ; Species ; Variation ; Vasopressin ; Vertebrates</subject><ispartof>PloS one, 2014-10, Vol.9 (10), p.e111638-e111638</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Ren et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Ren et al 2014 Ren et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c593t-94a2f49da4893a3755ce93e6ed40c21a28c33dc518e01e6e8d4bf1d0e3b946e43</citedby><cites>FETCH-LOGICAL-c593t-94a2f49da4893a3755ce93e6ed40c21a28c33dc518e01e6e8d4bf1d0e3b946e43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4216101/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4216101/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,861,882,2096,2915,23847,27905,27906,53772,53774,79349,79350</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25360668$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Vaudry, Hubert</contributor><creatorcontrib>Ren, Dongren</creatorcontrib><creatorcontrib>Chin, Kelvin R</creatorcontrib><creatorcontrib>French, Jeffrey A</creatorcontrib><title>Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>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.</description><subject>Amino acids</subject><subject>Animals</subject><subject>Arginine Vasopressin - genetics</subject><subject>Argipressin</subject><subject>Behavior, Animal</subject><subject>Binding</subject><subject>Biological Evolution</subject><subject>Biology</subject><subject>Biology and life sciences</subject><subject>C-Terminus</subject><subject>Coding</subject><subject>Evolution</subject><subject>Gene expression</subject><subject>Genera</subject><subject>Genetic diversity</subject><subject>Genetic Variation</subject><subject>Hormones</subject><subject>Humans</subject><subject>Kinases</subject><subject>Ligands</subject><subject>Mammals</subject><subject>Microtus</subject><subject>Models, Molecular</subject><subject>Molecular modelling</subject><subject>Molecular Sequence Data</subject><subject>Monkeys</subject><subject>Monogamy</subject><subject>N-Terminus</subject><subject>Neuropeptides</subject><subject>Non-coding RNA</subject><subject>Open Reading Frames - genetics</subject><subject>Oxytocin</subject><subject>Peromyscus</subject><subject>Phylogeny</subject><subject>Pituitary (posterior)</subject><subject>Pituitary hormones</subject><subject>Platyrrhini - genetics</subject><subject>Positive selection</subject><subject>Primates</subject><subject>Protein binding</subject><subject>Proteins</subject><subject>Receptors, Vasopressin - genetics</subject><subject>Rodentia</subject><subject>Rodents</subject><subject>Saimiri</subject><subject>Signal transduction</subject><subject>Social aspects</subject><subject>Social Behavior</subject><subject>Species</subject><subject>Variation</subject><subject>Vasopressin</subject><subject>Vertebrates</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptkttuEzEQhlcIREvhDRCsxE2RSPBpnTUXSFHFoVKBCHG4tCbe2dTFuw72blBueXK8ybZqUOWLscb_fDNj_Vn2lJIp5TP6-sr3oQU3XfsWp4RSKnl5LzumirOJZITfv3U_yh7FeEVIwUspH2ZHrOCSSFkeZ38_eYemdxDyDQQLnfVtbtt8_mORQ1sN8SuFIfMZ_-Q_fXBV3vj2F25jfroItoEO46t84aDbhnBpW_vyTY4b7_odaUDYZu2s2ZFjXvuQR28suAHjV9BsH2cPanARn4zxJPv-_t23s4-Tiy8fzs_mFxNTKN5NlABWC1WBKBUHPisKg4qjxEoQwyiw0nBemYKWSGhKl5VY1rQiyJdKSBT8JHu-566dj3r8vqippIqUQnGVFOd7ReXhSq-H7cJWe7B6l_BhpSF01jjUtGQEmSopLWuBNSrBJHBQignO5WyZWG_Hbv2ywcpg2wVwB9DDl9Ze6pXfaMHSRIQmwOkICP53j7HTjY0GnYMWfT_MzQhhopAkSV_8J717u1G1grSAbWuf-poBqueCzqgoKB_aTu9QpVNhY03yWm1T_qBA7AtM8DEGrG92pEQPTr0eRg9O1aNTU9mz2_9zU3RtTf4PQfXlbg</recordid><startdate>20141031</startdate><enddate>20141031</enddate><creator>Ren, Dongren</creator><creator>Chin, Kelvin R</creator><creator>French, Jeffrey A</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20141031</creationdate><title>Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy</title><author>Ren, Dongren ; Chin, Kelvin R ; French, Jeffrey A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c593t-94a2f49da4893a3755ce93e6ed40c21a28c33dc518e01e6e8d4bf1d0e3b946e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Amino acids</topic><topic>Animals</topic><topic>Arginine Vasopressin - genetics</topic><topic>Argipressin</topic><topic>Behavior, Animal</topic><topic>Binding</topic><topic>Biological Evolution</topic><topic>Biology</topic><topic>Biology and life sciences</topic><topic>C-Terminus</topic><topic>Coding</topic><topic>Evolution</topic><topic>Gene expression</topic><topic>Genera</topic><topic>Genetic diversity</topic><topic>Genetic Variation</topic><topic>Hormones</topic><topic>Humans</topic><topic>Kinases</topic><topic>Ligands</topic><topic>Mammals</topic><topic>Microtus</topic><topic>Models, Molecular</topic><topic>Molecular modelling</topic><topic>Molecular Sequence Data</topic><topic>Monkeys</topic><topic>Monogamy</topic><topic>N-Terminus</topic><topic>Neuropeptides</topic><topic>Non-coding RNA</topic><topic>Open Reading Frames - genetics</topic><topic>Oxytocin</topic><topic>Peromyscus</topic><topic>Phylogeny</topic><topic>Pituitary (posterior)</topic><topic>Pituitary hormones</topic><topic>Platyrrhini - genetics</topic><topic>Positive selection</topic><topic>Primates</topic><topic>Protein binding</topic><topic>Proteins</topic><topic>Receptors, Vasopressin - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ren, Dongren</au><au>Chin, Kelvin R</au><au>French, Jeffrey A</au><au>Vaudry, Hubert</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-10-31</date><risdate>2014</risdate><volume>9</volume><issue>10</issue><spage>e111638</spage><epage>e111638</epage><pages>e111638-e111638</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><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.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25360668</pmid><doi>10.1371/journal.pone.0111638</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Amino acids Animals Arginine Vasopressin - genetics Argipressin Behavior, Animal Binding Biological Evolution Biology Biology and life sciences C-Terminus Coding Evolution Gene expression Genera Genetic diversity Genetic Variation Hormones Humans Kinases Ligands Mammals Microtus Models, Molecular Molecular modelling Molecular Sequence Data Monkeys Monogamy N-Terminus Neuropeptides Non-coding RNA Open Reading Frames - genetics Oxytocin Peromyscus Phylogeny Pituitary (posterior) Pituitary hormones Platyrrhini - genetics Positive selection Primates Protein binding Proteins Receptors, Vasopressin - genetics Rodentia Rodents Saimiri Signal transduction Social aspects Social Behavior Species Variation Vasopressin Vertebrates |
| title | Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-19T13%3A12%3A12IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Molecular%20variation%20in%20AVP%20and%20AVPR1a%20in%20New%20World%20monkeys%20(Primates,%20Platyrrhini):%20evolution%20and%20implications%20for%20social%20monogamy&rft.jtitle=PloS%20one&rft.au=Ren,%20Dongren&rft.date=2014-10-31&rft.volume=9&rft.issue=10&rft.spage=e111638&rft.epage=e111638&rft.pages=e111638-e111638&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0111638&rft_dat=%3Cgale_plos_%3EA417145131%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1619084939&rft_id=info:pmid/25360668&rft_galeid=A417145131&rft_doaj_id=oai_doaj_org_article_1820e298118f4efe9426a3a99243367b&rfr_iscdi=true |