The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila
Sexually dimorphic traits play key roles in animal evolution and behavior. Little is known, however, about the mechanisms governing their development and evolution. One recently evolved dimorphic trait is the male-specific abdominal pigmentation of Drosophila melanogaster, which is repressed in fema...
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Veröffentlicht in: | Cell 2008-08, Vol.134 (4), p.610-623 |
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description | Sexually dimorphic traits play key roles in animal evolution and behavior. Little is known, however, about the mechanisms governing their development and evolution. One recently evolved dimorphic trait is the male-specific abdominal pigmentation of Drosophila melanogaster, which is repressed in females by the Bric-à-brac (Bab) proteins. To understand the regulation and origin of this trait, we have identified and traced the evolution of the genetic switch controlling dimorphic bab expression. We show that the HOX protein Abdominal-B (ABD-B) and the sex-specific isoforms of Doublesex (DSX) directly regulate a bab cis-regulatory element (CRE). In females, ABD-B and DSXF activate bab expression whereas in males DSXM directly represses bab, which allows for pigmentation. A new domain of dimorphic bab expression evolved through multiple fine-scale changes within this CRE, whose ancestral role was to regulate other dimorphic features. These findings reveal how new dimorphic characters can emerge from genetic networks regulating pre-existing dimorphic traits. |
doi_str_mv | 10.1016/j.cell.2008.06.052 |
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Little is known, however, about the mechanisms governing their development and evolution. One recently evolved dimorphic trait is the male-specific abdominal pigmentation of Drosophila melanogaster, which is repressed in females by the Bric-à-brac (Bab) proteins. To understand the regulation and origin of this trait, we have identified and traced the evolution of the genetic switch controlling dimorphic bab expression. We show that the HOX protein Abdominal-B (ABD-B) and the sex-specific isoforms of Doublesex (DSX) directly regulate a bab cis-regulatory element (CRE). In females, ABD-B and DSXF activate bab expression whereas in males DSXM directly represses bab, which allows for pigmentation. A new domain of dimorphic bab expression evolved through multiple fine-scale changes within this CRE, whose ancestral role was to regulate other dimorphic features. These findings reveal how new dimorphic characters can emerge from genetic networks regulating pre-existing dimorphic traits.</description><identifier>ISSN: 0092-8674</identifier><identifier>EISSN: 1097-4172</identifier><identifier>DOI: 10.1016/j.cell.2008.06.052</identifier><identifier>PMID: 18724934</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cellular Biology ; DEVBIO ; DNA ; DNA-Binding Proteins - metabolism ; Drosophila melanogaster ; Drosophila melanogaster - genetics ; Drosophila melanogaster - physiology ; Drosophila Proteins - metabolism ; EVO_ECOL ; Evolution, Molecular ; Female ; Gene Expression Regulation ; Homeodomain Proteins - metabolism ; Life Sciences ; Male ; Sex Characteristics ; Transcription Factors - metabolism</subject><ispartof>Cell, 2008-08, Vol.134 (4), p.610-623</ispartof><rights>2008 Elsevier Inc.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c584t-7544c0abbe529abc39da0ac9cd4b7506d6da9e64705d2b2ca4b40d41163ed07a3</citedby><cites>FETCH-LOGICAL-c584t-7544c0abbe529abc39da0ac9cd4b7506d6da9e64705d2b2ca4b40d41163ed07a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0092867408008404$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18724934$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-00312724$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Williams, Thomas M.</creatorcontrib><creatorcontrib>Selegue, Jane E.</creatorcontrib><creatorcontrib>Werner, Thomas</creatorcontrib><creatorcontrib>Gompel, Nicolas</creatorcontrib><creatorcontrib>Kopp, Artyom</creatorcontrib><creatorcontrib>Carroll, Sean B.</creatorcontrib><title>The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila</title><title>Cell</title><addtitle>Cell</addtitle><description>Sexually dimorphic traits play key roles in animal evolution and behavior. Little is known, however, about the mechanisms governing their development and evolution. One recently evolved dimorphic trait is the male-specific abdominal pigmentation of Drosophila melanogaster, which is repressed in females by the Bric-à-brac (Bab) proteins. To understand the regulation and origin of this trait, we have identified and traced the evolution of the genetic switch controlling dimorphic bab expression. We show that the HOX protein Abdominal-B (ABD-B) and the sex-specific isoforms of Doublesex (DSX) directly regulate a bab cis-regulatory element (CRE). In females, ABD-B and DSXF activate bab expression whereas in males DSXM directly represses bab, which allows for pigmentation. A new domain of dimorphic bab expression evolved through multiple fine-scale changes within this CRE, whose ancestral role was to regulate other dimorphic features. These findings reveal how new dimorphic characters can emerge from genetic networks regulating pre-existing dimorphic traits.</description><subject>Animals</subject><subject>Cellular Biology</subject><subject>DEVBIO</subject><subject>DNA</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - genetics</subject><subject>Drosophila melanogaster - physiology</subject><subject>Drosophila Proteins - metabolism</subject><subject>EVO_ECOL</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Gene Expression Regulation</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Sex Characteristics</subject><subject>Transcription Factors - metabolism</subject><issn>0092-8674</issn><issn>1097-4172</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUuP0zAUhSMEYsrAH2CBvEKaRcK149i1hJBGnRdSJSSmrC3HdhtXblzspDD_Hmda8VrAyvL1d869vqcoXmOoMGD2bltp631FAOYVsAoa8qSYYRC8pJiTp8UMQJByzjg9K16ktIUMNk3zvDjDc06oqOmsMKvOos92M3o1uNAj1Rt0fQh-fLyFNVLo1vZ2cBrdf3OD7tAi9EMM3rt-g-7t91F5_4Cu3C7EfZepVVRuSMj16CqGFHLNq5fFs7Xyyb46nefFl5vr1eKuXH66_bi4XJa6mdOh5A2lGlTb2oYI1epaGAVKC21oyxtghhklLKMcGkNaohVtKRiKMautAa7q8-LD0Xc_tjtrtM2TKi_30e1UfJBBOfnnS-86uQkHSRrBsZhng4ujQfeX7O5yKacaQI1J3t0BZ_btqVkMX0ebBrlzaQpE9TaMSTJBGQVG_gsSEFTwenIkR1DnzaVo1z9HwCCnxOVWTjo5JS6ByZx4Fr35_c-_JKeIM_D-CNi8-YOzUSbtbK-tcdHqQZrg_uX_A7mHvlo</recordid><startdate>20080822</startdate><enddate>20080822</enddate><creator>Williams, Thomas M.</creator><creator>Selegue, Jane E.</creator><creator>Werner, Thomas</creator><creator>Gompel, Nicolas</creator><creator>Kopp, Artyom</creator><creator>Carroll, Sean B.</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><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>7SS</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope></search><sort><creationdate>20080822</creationdate><title>The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila</title><author>Williams, Thomas M. ; Selegue, Jane E. ; Werner, Thomas ; Gompel, Nicolas ; Kopp, Artyom ; Carroll, Sean B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c584t-7544c0abbe529abc39da0ac9cd4b7506d6da9e64705d2b2ca4b40d41163ed07a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Animals</topic><topic>Cellular Biology</topic><topic>DEVBIO</topic><topic>DNA</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - genetics</topic><topic>Drosophila melanogaster - physiology</topic><topic>Drosophila Proteins - metabolism</topic><topic>EVO_ECOL</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Gene Expression Regulation</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Life Sciences</topic><topic>Male</topic><topic>Sex Characteristics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Williams, Thomas M.</creatorcontrib><creatorcontrib>Selegue, Jane E.</creatorcontrib><creatorcontrib>Werner, Thomas</creatorcontrib><creatorcontrib>Gompel, Nicolas</creatorcontrib><creatorcontrib>Kopp, Artyom</creatorcontrib><creatorcontrib>Carroll, Sean B.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Williams, Thomas M.</au><au>Selegue, Jane E.</au><au>Werner, Thomas</au><au>Gompel, Nicolas</au><au>Kopp, Artyom</au><au>Carroll, Sean B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila</atitle><jtitle>Cell</jtitle><addtitle>Cell</addtitle><date>2008-08-22</date><risdate>2008</risdate><volume>134</volume><issue>4</issue><spage>610</spage><epage>623</epage><pages>610-623</pages><issn>0092-8674</issn><eissn>1097-4172</eissn><abstract>Sexually dimorphic traits play key roles in animal evolution and behavior. Little is known, however, about the mechanisms governing their development and evolution. One recently evolved dimorphic trait is the male-specific abdominal pigmentation of Drosophila melanogaster, which is repressed in females by the Bric-à-brac (Bab) proteins. To understand the regulation and origin of this trait, we have identified and traced the evolution of the genetic switch controlling dimorphic bab expression. We show that the HOX protein Abdominal-B (ABD-B) and the sex-specific isoforms of Doublesex (DSX) directly regulate a bab cis-regulatory element (CRE). In females, ABD-B and DSXF activate bab expression whereas in males DSXM directly represses bab, which allows for pigmentation. A new domain of dimorphic bab expression evolved through multiple fine-scale changes within this CRE, whose ancestral role was to regulate other dimorphic features. 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subjects | Animals Cellular Biology DEVBIO DNA DNA-Binding Proteins - metabolism Drosophila melanogaster Drosophila melanogaster - genetics Drosophila melanogaster - physiology Drosophila Proteins - metabolism EVO_ECOL Evolution, Molecular Female Gene Expression Regulation Homeodomain Proteins - metabolism Life Sciences Male Sex Characteristics Transcription Factors - metabolism |
title | The Regulation and Evolution of a Genetic Switch Controlling Sexually Dimorphic Traits in Drosophila |
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