Evolution of a novel adrenal cell type that promotes parental care
Cell types with specialized functions fundamentally regulate animal behaviour, and yet the genetic mechanisms that underlie the emergence of novel cell types and their consequences for behaviour are not well understood 1 . Here we show that the monogamous oldfield mouse ( Peromyscus polionotus ) has...
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creator | Niepoth, Natalie Merritt, Jennifer R. Uminski, Michelle Lei, Emily Esquibies, Victoria S. Bando, Ina B. Hernandez, Kimberly Gebhardt, Christoph Wacker, Sarah A. Lutzu, Stefano Poudel, Asmita Soma, Kiran K. Rudolph, Stephanie Bendesky, Andres |
description | Cell types with specialized functions fundamentally regulate animal behaviour, and yet the genetic mechanisms that underlie the emergence of novel cell types and their consequences for behaviour are not well understood
1
. Here we show that the monogamous oldfield mouse (
Peromyscus polionotus
) has recently evolved a novel cell type in the adrenal gland that expresses the enzyme AKR1C18, which converts progesterone into 20α-hydroxyprogesterone. We then demonstrate that 20α-hydroxyprogesterone is more abundant in oldfield mice, where it induces monogamous-typical parental behaviours, than in the closely related promiscuous deer mice (
Peromyscus maniculatus
). Using quantitative trait locus mapping in a cross between these species, we ultimately find interspecific genetic variation that drives expression of the nuclear protein GADD45A and the glycoprotein tenascin N, which contribute to the emergence and function of this cell type in oldfield mice. Our results provide an example by which the recent evolution of a new cell type in a gland outside the brain contributes to the evolution of social behaviour.
The adrenal gland of the oldfield mouse (
Peromyscus polionotus
) has a recently evolved cell type that promotes monogamous-typical parenting behaviour and is not present in closely related species. |
doi_str_mv | 10.1038/s41586-024-07423-y |
format | Article |
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1
. Here we show that the monogamous oldfield mouse (
Peromyscus polionotus
) has recently evolved a novel cell type in the adrenal gland that expresses the enzyme AKR1C18, which converts progesterone into 20α-hydroxyprogesterone. We then demonstrate that 20α-hydroxyprogesterone is more abundant in oldfield mice, where it induces monogamous-typical parental behaviours, than in the closely related promiscuous deer mice (
Peromyscus maniculatus
). Using quantitative trait locus mapping in a cross between these species, we ultimately find interspecific genetic variation that drives expression of the nuclear protein GADD45A and the glycoprotein tenascin N, which contribute to the emergence and function of this cell type in oldfield mice. Our results provide an example by which the recent evolution of a new cell type in a gland outside the brain contributes to the evolution of social behaviour.
The adrenal gland of the oldfield mouse (
Peromyscus polionotus
) has a recently evolved cell type that promotes monogamous-typical parenting behaviour and is not present in closely related species.</description><identifier>ISSN: 0028-0836</identifier><identifier>ISSN: 1476-4687</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-024-07423-y</identifier><identifier>PMID: 38750354</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>20-alpha-Dihydroprogesterone - metabolism ; 38 ; 38/23 ; 38/91 ; 631/181/2469 ; 631/181/2474 ; 631/181/2806 ; 631/378/3919 ; Adrenal glands ; Adrenal Glands - cytology ; Adrenal Glands - enzymology ; Adrenal Glands - metabolism ; Animals ; Behavior ; Biological Evolution ; Catecholamines ; Enzymes ; Estradiol Dehydrogenases - genetics ; Estradiol Dehydrogenases - metabolism ; Evolution ; Female ; Females ; GADD45 Proteins - genetics ; Gadd45A protein ; Gene mapping ; Genes ; Genetic diversity ; Genetic Variation ; Glycoproteins ; Hormones ; Humanities and Social Sciences ; Hybridization, Genetic ; Male ; Monogamy ; multidisciplinary ; Parental behavior ; Parents & parenting ; Paternal Behavior ; Peromyscus - classification ; Peromyscus - genetics ; Peromyscus - physiology ; Physiology ; Predation ; Progesterone ; Progesterone - metabolism ; Quantitative genetics ; Quantitative Trait Loci ; Science ; Science (multidisciplinary) ; Small mammals ; Social Behavior ; Steroids ; Tenascin ; Tenascin - genetics</subject><ispartof>Nature (London), 2024-05, Vol.629 (8014), p.1082-1090</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Springer Nature Limited.</rights><rights>Copyright Nature Publishing Group May 30, 2024</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-3e68769c451b5e29adf0b1a2959d2e47eb6823ecf12d38e27bbaab5cfb81342c3</citedby><cites>FETCH-LOGICAL-c475t-3e68769c451b5e29adf0b1a2959d2e47eb6823ecf12d38e27bbaab5cfb81342c3</cites><orcidid>0000-0001-7926-4487 ; 0000-0001-8057-8977 ; 0000-0002-4220-3653 ; 0009-0004-7952-8090</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-024-07423-y$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-024-07423-y$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38750354$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Niepoth, Natalie</creatorcontrib><creatorcontrib>Merritt, Jennifer R.</creatorcontrib><creatorcontrib>Uminski, Michelle</creatorcontrib><creatorcontrib>Lei, Emily</creatorcontrib><creatorcontrib>Esquibies, Victoria S.</creatorcontrib><creatorcontrib>Bando, Ina B.</creatorcontrib><creatorcontrib>Hernandez, Kimberly</creatorcontrib><creatorcontrib>Gebhardt, Christoph</creatorcontrib><creatorcontrib>Wacker, Sarah A.</creatorcontrib><creatorcontrib>Lutzu, Stefano</creatorcontrib><creatorcontrib>Poudel, Asmita</creatorcontrib><creatorcontrib>Soma, Kiran K.</creatorcontrib><creatorcontrib>Rudolph, Stephanie</creatorcontrib><creatorcontrib>Bendesky, Andres</creatorcontrib><title>Evolution of a novel adrenal cell type that promotes parental care</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Cell types with specialized functions fundamentally regulate animal behaviour, and yet the genetic mechanisms that underlie the emergence of novel cell types and their consequences for behaviour are not well understood
1
. Here we show that the monogamous oldfield mouse (
Peromyscus polionotus
) has recently evolved a novel cell type in the adrenal gland that expresses the enzyme AKR1C18, which converts progesterone into 20α-hydroxyprogesterone. We then demonstrate that 20α-hydroxyprogesterone is more abundant in oldfield mice, where it induces monogamous-typical parental behaviours, than in the closely related promiscuous deer mice (
Peromyscus maniculatus
). Using quantitative trait locus mapping in a cross between these species, we ultimately find interspecific genetic variation that drives expression of the nuclear protein GADD45A and the glycoprotein tenascin N, which contribute to the emergence and function of this cell type in oldfield mice. Our results provide an example by which the recent evolution of a new cell type in a gland outside the brain contributes to the evolution of social behaviour.
The adrenal gland of the oldfield mouse (
Peromyscus polionotus
) has a recently evolved cell type that promotes monogamous-typical parenting behaviour and is not present in closely related species.</description><subject>20-alpha-Dihydroprogesterone - metabolism</subject><subject>38</subject><subject>38/23</subject><subject>38/91</subject><subject>631/181/2469</subject><subject>631/181/2474</subject><subject>631/181/2806</subject><subject>631/378/3919</subject><subject>Adrenal glands</subject><subject>Adrenal Glands - cytology</subject><subject>Adrenal Glands - enzymology</subject><subject>Adrenal Glands - metabolism</subject><subject>Animals</subject><subject>Behavior</subject><subject>Biological Evolution</subject><subject>Catecholamines</subject><subject>Enzymes</subject><subject>Estradiol Dehydrogenases - genetics</subject><subject>Estradiol Dehydrogenases - metabolism</subject><subject>Evolution</subject><subject>Female</subject><subject>Females</subject><subject>GADD45 Proteins - genetics</subject><subject>Gadd45A protein</subject><subject>Gene mapping</subject><subject>Genes</subject><subject>Genetic diversity</subject><subject>Genetic Variation</subject><subject>Glycoproteins</subject><subject>Hormones</subject><subject>Humanities and Social Sciences</subject><subject>Hybridization, Genetic</subject><subject>Male</subject><subject>Monogamy</subject><subject>multidisciplinary</subject><subject>Parental behavior</subject><subject>Parents & parenting</subject><subject>Paternal Behavior</subject><subject>Peromyscus - classification</subject><subject>Peromyscus - genetics</subject><subject>Peromyscus - physiology</subject><subject>Physiology</subject><subject>Predation</subject><subject>Progesterone</subject><subject>Progesterone - metabolism</subject><subject>Quantitative genetics</subject><subject>Quantitative Trait Loci</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Small mammals</subject><subject>Social Behavior</subject><subject>Steroids</subject><subject>Tenascin</subject><subject>Tenascin - genetics</subject><issn>0028-0836</issn><issn>1476-4687</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtLxDAUhYMozvj4Ay4k4MZNNc8mXYkOvmDAja5D2t5qpdPUpB2Yf2_qjM-FZJHA-e659-YgdETJGSVcnwdBpU4TwkRClGA8WW2hKRUqTUSq1TaaEsJ0QjRPJ2gvhFdCiKRK7KIJ10oSLsUUXV0vXTP0tWuxq7DFrVtCg23pobUNLqBpcL_qAPcvtseddwvXQ8CdjXo_AvFxgHYq2wQ43Nz76Onm-nF2l8wfbu9nl_OkEEr2CYc4VJoVQtJcAstsWZGcWpbJrGQgFOSpZhyKirKSa2Aqz63NZVHlmnLBCr6PLta-3ZAvoCziBN42pvP1wvqVcbY2v5W2fjHPbmko5SyLJzqcbhy8exsg9GZRh3FH24IbguFESp1xyUb05A_66gYf_2SkUq6yjKUkUmxNFd6F4KH6moYSM2Zk1hmZmJH5yMisYtHxzz2-Sj5DiQBfAyFK7TP4797_2L4D0rGd2g</recordid><startdate>20240530</startdate><enddate>20240530</enddate><creator>Niepoth, Natalie</creator><creator>Merritt, Jennifer R.</creator><creator>Uminski, Michelle</creator><creator>Lei, Emily</creator><creator>Esquibies, Victoria S.</creator><creator>Bando, Ina B.</creator><creator>Hernandez, Kimberly</creator><creator>Gebhardt, Christoph</creator><creator>Wacker, Sarah A.</creator><creator>Lutzu, Stefano</creator><creator>Poudel, Asmita</creator><creator>Soma, Kiran K.</creator><creator>Rudolph, Stephanie</creator><creator>Bendesky, Andres</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>KL.</scope><scope>M7N</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7926-4487</orcidid><orcidid>https://orcid.org/0000-0001-8057-8977</orcidid><orcidid>https://orcid.org/0000-0002-4220-3653</orcidid><orcidid>https://orcid.org/0009-0004-7952-8090</orcidid></search><sort><creationdate>20240530</creationdate><title>Evolution of a novel adrenal cell type that promotes parental care</title><author>Niepoth, Natalie ; Merritt, Jennifer R. ; Uminski, Michelle ; Lei, Emily ; Esquibies, Victoria S. ; Bando, Ina B. ; Hernandez, Kimberly ; Gebhardt, Christoph ; Wacker, Sarah A. ; Lutzu, Stefano ; Poudel, Asmita ; Soma, Kiran K. ; Rudolph, Stephanie ; Bendesky, Andres</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c475t-3e68769c451b5e29adf0b1a2959d2e47eb6823ecf12d38e27bbaab5cfb81342c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>20-alpha-Dihydroprogesterone - metabolism</topic><topic>38</topic><topic>38/23</topic><topic>38/91</topic><topic>631/181/2469</topic><topic>631/181/2474</topic><topic>631/181/2806</topic><topic>631/378/3919</topic><topic>Adrenal glands</topic><topic>Adrenal Glands - cytology</topic><topic>Adrenal Glands - enzymology</topic><topic>Adrenal Glands - metabolism</topic><topic>Animals</topic><topic>Behavior</topic><topic>Biological Evolution</topic><topic>Catecholamines</topic><topic>Enzymes</topic><topic>Estradiol Dehydrogenases - genetics</topic><topic>Estradiol Dehydrogenases - metabolism</topic><topic>Evolution</topic><topic>Female</topic><topic>Females</topic><topic>GADD45 Proteins - genetics</topic><topic>Gadd45A protein</topic><topic>Gene mapping</topic><topic>Genes</topic><topic>Genetic diversity</topic><topic>Genetic Variation</topic><topic>Glycoproteins</topic><topic>Hormones</topic><topic>Humanities and Social Sciences</topic><topic>Hybridization, Genetic</topic><topic>Male</topic><topic>Monogamy</topic><topic>multidisciplinary</topic><topic>Parental behavior</topic><topic>Parents & parenting</topic><topic>Paternal Behavior</topic><topic>Peromyscus - classification</topic><topic>Peromyscus - genetics</topic><topic>Peromyscus - physiology</topic><topic>Physiology</topic><topic>Predation</topic><topic>Progesterone</topic><topic>Progesterone - metabolism</topic><topic>Quantitative genetics</topic><topic>Quantitative Trait Loci</topic><topic>Science</topic><topic>Science (multidisciplinary)</topic><topic>Small mammals</topic><topic>Social Behavior</topic><topic>Steroids</topic><topic>Tenascin</topic><topic>Tenascin - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Niepoth, Natalie</creatorcontrib><creatorcontrib>Merritt, Jennifer R.</creatorcontrib><creatorcontrib>Uminski, Michelle</creatorcontrib><creatorcontrib>Lei, Emily</creatorcontrib><creatorcontrib>Esquibies, Victoria S.</creatorcontrib><creatorcontrib>Bando, Ina B.</creatorcontrib><creatorcontrib>Hernandez, Kimberly</creatorcontrib><creatorcontrib>Gebhardt, Christoph</creatorcontrib><creatorcontrib>Wacker, Sarah A.</creatorcontrib><creatorcontrib>Lutzu, Stefano</creatorcontrib><creatorcontrib>Poudel, Asmita</creatorcontrib><creatorcontrib>Soma, Kiran K.</creatorcontrib><creatorcontrib>Rudolph, Stephanie</creatorcontrib><creatorcontrib>Bendesky, Andres</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Meteorological & Geoastrophysical Abstracts - Academic</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Niepoth, Natalie</au><au>Merritt, Jennifer R.</au><au>Uminski, Michelle</au><au>Lei, Emily</au><au>Esquibies, Victoria S.</au><au>Bando, Ina B.</au><au>Hernandez, Kimberly</au><au>Gebhardt, Christoph</au><au>Wacker, Sarah A.</au><au>Lutzu, Stefano</au><au>Poudel, Asmita</au><au>Soma, Kiran K.</au><au>Rudolph, Stephanie</au><au>Bendesky, Andres</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolution of a novel adrenal cell type that promotes parental care</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2024-05-30</date><risdate>2024</risdate><volume>629</volume><issue>8014</issue><spage>1082</spage><epage>1090</epage><pages>1082-1090</pages><issn>0028-0836</issn><issn>1476-4687</issn><eissn>1476-4687</eissn><abstract>Cell types with specialized functions fundamentally regulate animal behaviour, and yet the genetic mechanisms that underlie the emergence of novel cell types and their consequences for behaviour are not well understood
1
. Here we show that the monogamous oldfield mouse (
Peromyscus polionotus
) has recently evolved a novel cell type in the adrenal gland that expresses the enzyme AKR1C18, which converts progesterone into 20α-hydroxyprogesterone. We then demonstrate that 20α-hydroxyprogesterone is more abundant in oldfield mice, where it induces monogamous-typical parental behaviours, than in the closely related promiscuous deer mice (
Peromyscus maniculatus
). Using quantitative trait locus mapping in a cross between these species, we ultimately find interspecific genetic variation that drives expression of the nuclear protein GADD45A and the glycoprotein tenascin N, which contribute to the emergence and function of this cell type in oldfield mice. Our results provide an example by which the recent evolution of a new cell type in a gland outside the brain contributes to the evolution of social behaviour.
The adrenal gland of the oldfield mouse (
Peromyscus polionotus
) has a recently evolved cell type that promotes monogamous-typical parenting behaviour and is not present in closely related species.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>38750354</pmid><doi>10.1038/s41586-024-07423-y</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0001-7926-4487</orcidid><orcidid>https://orcid.org/0000-0001-8057-8977</orcidid><orcidid>https://orcid.org/0000-0002-4220-3653</orcidid><orcidid>https://orcid.org/0009-0004-7952-8090</orcidid><oa>free_for_read</oa></addata></record> |
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ispartof | Nature (London), 2024-05, Vol.629 (8014), p.1082-1090 |
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language | eng |
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source | MEDLINE; Nature Journals Online; SpringerLink Journals - AutoHoldings |
subjects | 20-alpha-Dihydroprogesterone - metabolism 38 38/23 38/91 631/181/2469 631/181/2474 631/181/2806 631/378/3919 Adrenal glands Adrenal Glands - cytology Adrenal Glands - enzymology Adrenal Glands - metabolism Animals Behavior Biological Evolution Catecholamines Enzymes Estradiol Dehydrogenases - genetics Estradiol Dehydrogenases - metabolism Evolution Female Females GADD45 Proteins - genetics Gadd45A protein Gene mapping Genes Genetic diversity Genetic Variation Glycoproteins Hormones Humanities and Social Sciences Hybridization, Genetic Male Monogamy multidisciplinary Parental behavior Parents & parenting Paternal Behavior Peromyscus - classification Peromyscus - genetics Peromyscus - physiology Physiology Predation Progesterone Progesterone - metabolism Quantitative genetics Quantitative Trait Loci Science Science (multidisciplinary) Small mammals Social Behavior Steroids Tenascin Tenascin - genetics |
title | Evolution of a novel adrenal cell type that promotes parental care |
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