Evolutionary patterns of major urinary protein scent signals in house mice and relatives
Scent marks are important mediators of territorial behaviour and sexual selection, especially among mammals. The evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of ch...
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Veröffentlicht in: | Molecular ecology 2019-08, Vol.28 (15), p.3587-3601 |
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description | Scent marks are important mediators of territorial behaviour and sexual selection, especially among mammals. The evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here, we examine the evolution of urinary protein signals among house mice and relatives by examining the sequences and patterns of mRNA expression of Mup genes related to urinary scent marks. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, protein scent signals that are male specific in well‐studied inbred laboratory strains vary in sex‐specificity among species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that chemosensory perception may have played a major role in shaping MUP diversity. These data highlight diverse processes and pressures shaping scent signals, and suggest new avenues for using wild mice to probe the evolution of signals and signal processing. |
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The evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here, we examine the evolution of urinary protein signals among house mice and relatives by examining the sequences and patterns of mRNA expression of Mup genes related to urinary scent marks. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, protein scent signals that are male specific in well‐studied inbred laboratory strains vary in sex‐specificity among species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that chemosensory perception may have played a major role in shaping MUP diversity. These data highlight diverse processes and pressures shaping scent signals, and suggest new avenues for using wild mice to probe the evolution of signals and signal processing.</description><identifier>ISSN: 0962-1083</identifier><identifier>EISSN: 1365-294X</identifier><identifier>DOI: 10.1111/mec.15155</identifier><identifier>PMID: 31232499</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Acids ; Amino acids ; Animals ; Base Sequence ; Biological evolution ; Chemical communication ; Chemoreception ; commensalism ; domestication ; Evolution ; Evolution, Molecular ; Female ; Gene duplication ; Gene expression ; Gene Expression Regulation ; Gene sequencing ; Genes ; Genome ; Genotypes ; Inbreeding ; Liver - metabolism ; Male ; Mice ; Odorant receptors ; Odorants ; Organic chemistry ; Phenotypes ; pheromones ; Phylogeny ; Proteins ; Proteins - genetics ; Receptors ; rodent ; Scent marking behavior ; Sex ; Sexual behavior ; Sexual selection ; Signal processing ; social evolution ; social neuroscience ; Species Specificity ; Territorial behavior ; Vomeronasal organ ; Vomeronasal system</subject><ispartof>Molecular ecology, 2019-08, Vol.28 (15), p.3587-3601</ispartof><rights>2019 John Wiley & Sons Ltd</rights><rights>2019 John Wiley & Sons Ltd.</rights><rights>Copyright © 2019 John Wiley & Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4195-bc6e0d8f3d46572ff985fa60d8c25d93d7a83c4e4b56b3be3742ff4f4e1e52223</citedby><cites>FETCH-LOGICAL-c4195-bc6e0d8f3d46572ff985fa60d8c25d93d7a83c4e4b56b3be3742ff4f4e1e52223</cites><orcidid>0000-0001-7660-9814 ; 0000-0002-3949-7873</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fmec.15155$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fmec.15155$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31232499$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sheehan, Michael J.</creatorcontrib><creatorcontrib>Campbell, Polly</creatorcontrib><creatorcontrib>Miller, Caitlin H.</creatorcontrib><title>Evolutionary patterns of major urinary protein scent signals in house mice and relatives</title><title>Molecular ecology</title><addtitle>Mol Ecol</addtitle><description>Scent marks are important mediators of territorial behaviour and sexual selection, especially among mammals. The evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here, we examine the evolution of urinary protein signals among house mice and relatives by examining the sequences and patterns of mRNA expression of Mup genes related to urinary scent marks. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, protein scent signals that are male specific in well‐studied inbred laboratory strains vary in sex‐specificity among species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that chemosensory perception may have played a major role in shaping MUP diversity. These data highlight diverse processes and pressures shaping scent signals, and suggest new avenues for using wild mice to probe the evolution of signals and signal processing.</description><subject>Acids</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Base Sequence</subject><subject>Biological evolution</subject><subject>Chemical communication</subject><subject>Chemoreception</subject><subject>commensalism</subject><subject>domestication</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Gene duplication</subject><subject>Gene expression</subject><subject>Gene Expression Regulation</subject><subject>Gene sequencing</subject><subject>Genes</subject><subject>Genome</subject><subject>Genotypes</subject><subject>Inbreeding</subject><subject>Liver - metabolism</subject><subject>Male</subject><subject>Mice</subject><subject>Odorant receptors</subject><subject>Odorants</subject><subject>Organic chemistry</subject><subject>Phenotypes</subject><subject>pheromones</subject><subject>Phylogeny</subject><subject>Proteins</subject><subject>Proteins - genetics</subject><subject>Receptors</subject><subject>rodent</subject><subject>Scent marking behavior</subject><subject>Sex</subject><subject>Sexual behavior</subject><subject>Sexual selection</subject><subject>Signal processing</subject><subject>social evolution</subject><subject>social neuroscience</subject><subject>Species Specificity</subject><subject>Territorial behavior</subject><subject>Vomeronasal organ</subject><subject>Vomeronasal system</subject><issn>0962-1083</issn><issn>1365-294X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10E1LwzAYB_AgipvTg19AAl700K15XXuUMV9A8aKwW0jTp5rRNjNpFb-9mZ0eBHMJPPnx58kfoVOSTkk8swbMlAgixB4aEyZFQnO-2kfjNJc0IWnGRugohHWaEkaFOEQjRiijPM_HaLV8d3XfWddq_4k3uuvAtwG7Cjd67TzuvR1evOvAtjgYaDsc7Eur64Dj4NX1AXBjDWDdlthDrTv7DuEYHVSRwMnunqDn6-XT4ja5f7y5W1zdJ4aTXCSFkZCWWcVKLsWcVlWeiUrLODJUlDkr5zpjhgMvhCxYAWzOI-IVBwKCUsom6GLIjRu-9RA61di4ZF3rFuJqilIuKRNUskjP_9C16_32I1FllKecsSyqy0EZ70LwUKmNt03sQJFUbetWsW71XXe0Z7vEvmig_JU__UYwG8CHreHz_yT1sFwMkV8fT4mX</recordid><startdate>201908</startdate><enddate>201908</enddate><creator>Sheehan, Michael J.</creator><creator>Campbell, Polly</creator><creator>Miller, Caitlin H.</creator><general>Blackwell Publishing Ltd</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>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7660-9814</orcidid><orcidid>https://orcid.org/0000-0002-3949-7873</orcidid></search><sort><creationdate>201908</creationdate><title>Evolutionary patterns of major urinary protein scent signals in house mice and relatives</title><author>Sheehan, Michael J. ; Campbell, Polly ; Miller, Caitlin H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4195-bc6e0d8f3d46572ff985fa60d8c25d93d7a83c4e4b56b3be3742ff4f4e1e52223</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Acids</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Base Sequence</topic><topic>Biological evolution</topic><topic>Chemical communication</topic><topic>Chemoreception</topic><topic>commensalism</topic><topic>domestication</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Gene duplication</topic><topic>Gene expression</topic><topic>Gene Expression Regulation</topic><topic>Gene sequencing</topic><topic>Genes</topic><topic>Genome</topic><topic>Genotypes</topic><topic>Inbreeding</topic><topic>Liver - metabolism</topic><topic>Male</topic><topic>Mice</topic><topic>Odorant receptors</topic><topic>Odorants</topic><topic>Organic chemistry</topic><topic>Phenotypes</topic><topic>pheromones</topic><topic>Phylogeny</topic><topic>Proteins</topic><topic>Proteins - genetics</topic><topic>Receptors</topic><topic>rodent</topic><topic>Scent marking behavior</topic><topic>Sex</topic><topic>Sexual behavior</topic><topic>Sexual selection</topic><topic>Signal processing</topic><topic>social evolution</topic><topic>social neuroscience</topic><topic>Species Specificity</topic><topic>Territorial behavior</topic><topic>Vomeronasal organ</topic><topic>Vomeronasal system</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sheehan, Michael J.</creatorcontrib><creatorcontrib>Campbell, Polly</creatorcontrib><creatorcontrib>Miller, Caitlin H.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sheehan, Michael J.</au><au>Campbell, Polly</au><au>Miller, Caitlin H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Evolutionary patterns of major urinary protein scent signals in house mice and relatives</atitle><jtitle>Molecular ecology</jtitle><addtitle>Mol Ecol</addtitle><date>2019-08</date><risdate>2019</risdate><volume>28</volume><issue>15</issue><spage>3587</spage><epage>3601</epage><pages>3587-3601</pages><issn>0962-1083</issn><eissn>1365-294X</eissn><abstract>Scent marks are important mediators of territorial behaviour and sexual selection, especially among mammals. The evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here, we examine the evolution of urinary protein signals among house mice and relatives by examining the sequences and patterns of mRNA expression of Mup genes related to urinary scent marks. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, protein scent signals that are male specific in well‐studied inbred laboratory strains vary in sex‐specificity among species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that chemosensory perception may have played a major role in shaping MUP diversity. These data highlight diverse processes and pressures shaping scent signals, and suggest new avenues for using wild mice to probe the evolution of signals and signal processing.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31232499</pmid><doi>10.1111/mec.15155</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0001-7660-9814</orcidid><orcidid>https://orcid.org/0000-0002-3949-7873</orcidid></addata></record> |
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subjects | Acids Amino acids Animals Base Sequence Biological evolution Chemical communication Chemoreception commensalism domestication Evolution Evolution, Molecular Female Gene duplication Gene expression Gene Expression Regulation Gene sequencing Genes Genome Genotypes Inbreeding Liver - metabolism Male Mice Odorant receptors Odorants Organic chemistry Phenotypes pheromones Phylogeny Proteins Proteins - genetics Receptors rodent Scent marking behavior Sex Sexual behavior Sexual selection Signal processing social evolution social neuroscience Species Specificity Territorial behavior Vomeronasal organ Vomeronasal system |
title | Evolutionary patterns of major urinary protein scent signals in house mice and relatives |
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