THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION
An important tenet of evolutionary developmental biology (“evo devo”) is that adaptive mutations affecting morphology are more likely to occur in the cis-regulatory regions than in the protein-coding regions of genes. This argument rests on two claims: (1) the modular nature of cis-regulatory elemen...
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Veröffentlicht in: | Evolution 2007-05, Vol.61 (5), p.995-1016 |
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description | An important tenet of evolutionary developmental biology (“evo devo”) is that adaptive mutations affecting morphology are more likely to occur in the cis-regulatory regions than in the protein-coding regions of genes. This argument rests on two claims: (1) the modular nature of cis-regulatory elements largely frees them from deleterious pleiotropic effects, and (2) a growing body of empirical evidence appears to support the predominant role of gene regulatory change in adaptation, especially morphological adaptation. Here we discuss and critique these assertions. We first show that there is no theoretical or empirical basis for the evo devo contention that adaptations involving morphology evolve by genetic mechanisms different from those involving physiology and other traits. In addition, some forms of protein evolution can avoid the negative consequences of pleiotropy, most notably via gene duplication. In light of evo devo claims, we then examine the substantial data on the genetic basis of adaptation from both genome-wide surveys and single-locus studies. Genomic studies lend little support to the cis-regulatory theory: many of these have detected adaptation in protein-coding regions, including transcription factors, whereas few have examined regulatory regions. Turning to single-locus studies, we note that the most widely cited examples of adaptive cis-regulatory mutations focus on trait loss rather than gain, and none have yet pinpointed an evolved regulatory site. In contrast, there are many studies that have both identified structural mutations and functionally verified their contribution to adaptation and speciation. Neither the theoretical arguments nor the data from nature, then, support the claim for a predominance of cis-regulatory mutations in evolution. Although this claim may be true, it is at best premature. Adaptation and speciation probably proceed through a combination of cis-regulatory and structural mutations, with a substantial contribution of the latter. |
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This argument rests on two claims: (1) the modular nature of cis-regulatory elements largely frees them from deleterious pleiotropic effects, and (2) a growing body of empirical evidence appears to support the predominant role of gene regulatory change in adaptation, especially morphological adaptation. Here we discuss and critique these assertions. We first show that there is no theoretical or empirical basis for the evo devo contention that adaptations involving morphology evolve by genetic mechanisms different from those involving physiology and other traits. In addition, some forms of protein evolution can avoid the negative consequences of pleiotropy, most notably via gene duplication. In light of evo devo claims, we then examine the substantial data on the genetic basis of adaptation from both genome-wide surveys and single-locus studies. Genomic studies lend little support to the cis-regulatory theory: many of these have detected adaptation in protein-coding regions, including transcription factors, whereas few have examined regulatory regions. Turning to single-locus studies, we note that the most widely cited examples of adaptive cis-regulatory mutations focus on trait loss rather than gain, and none have yet pinpointed an evolved regulatory site. In contrast, there are many studies that have both identified structural mutations and functionally verified their contribution to adaptation and speciation. Neither the theoretical arguments nor the data from nature, then, support the claim for a predominance of cis-regulatory mutations in evolution. Although this claim may be true, it is at best premature. Adaptation and speciation probably proceed through a combination of cis-regulatory and structural mutations, with a substantial contribution of the latter.</description><identifier>ISSN: 0014-3820</identifier><identifier>EISSN: 1558-5646</identifier><identifier>DOI: 10.1111/j.1558-5646.2007.00105.x</identifier><identifier>PMID: 17492956</identifier><language>eng</language><publisher>Malden, USA: Blackwell Science Inc</publisher><subject>Animals ; Biological adaptation ; Biological Evolution ; Cis-regulation ; Commentary ; DNA ; Drosophila ; Evolution ; evolution of development ; Evolutionary biology ; Evolutionary genetics ; gene regulation ; Genes ; Genetic mutation ; Genetics ; Genomics ; Morphogenesis - genetics ; Mutation ; phenotypic evolution ; Phenotypic traits ; Regulatory Elements, Transcriptional ; structural gene ; Transcription factors</subject><ispartof>Evolution, 2007-05, Vol.61 (5), p.995-1016</ispartof><rights>2007 The Author(s). Journal compilation © 2007 The Society for the Study of Evolution</rights><rights>Copyright 2007 The Society for the Study of Evolution</rights><rights>Copyright Society for the Study of Evolution May 2007</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b5125-c82a3462805546e6f9837d5cdbc201d8cb5b541f2ee8a571c3548411e935459b3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://bioone.org/doi/pdf/10.1111/j.1558-5646.2007.00105.x$$EPDF$$P50$$Gbioone$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/4621350$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,780,784,803,1417,26978,27924,27925,45574,45575,52363,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/17492956$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Rausher, M</contributor><creatorcontrib>Hoekstra, Hopi E.</creatorcontrib><creatorcontrib>Coyne, Jerry A.</creatorcontrib><title>THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION</title><title>Evolution</title><addtitle>Evolution</addtitle><description>An important tenet of evolutionary developmental biology (“evo devo”) is that adaptive mutations affecting morphology are more likely to occur in the cis-regulatory regions than in the protein-coding regions of genes. This argument rests on two claims: (1) the modular nature of cis-regulatory elements largely frees them from deleterious pleiotropic effects, and (2) a growing body of empirical evidence appears to support the predominant role of gene regulatory change in adaptation, especially morphological adaptation. Here we discuss and critique these assertions. We first show that there is no theoretical or empirical basis for the evo devo contention that adaptations involving morphology evolve by genetic mechanisms different from those involving physiology and other traits. In addition, some forms of protein evolution can avoid the negative consequences of pleiotropy, most notably via gene duplication. In light of evo devo claims, we then examine the substantial data on the genetic basis of adaptation from both genome-wide surveys and single-locus studies. Genomic studies lend little support to the cis-regulatory theory: many of these have detected adaptation in protein-coding regions, including transcription factors, whereas few have examined regulatory regions. Turning to single-locus studies, we note that the most widely cited examples of adaptive cis-regulatory mutations focus on trait loss rather than gain, and none have yet pinpointed an evolved regulatory site. In contrast, there are many studies that have both identified structural mutations and functionally verified their contribution to adaptation and speciation. Neither the theoretical arguments nor the data from nature, then, support the claim for a predominance of cis-regulatory mutations in evolution. Although this claim may be true, it is at best premature. Adaptation and speciation probably proceed through a combination of cis-regulatory and structural mutations, with a substantial contribution of the latter.</description><subject>Animals</subject><subject>Biological adaptation</subject><subject>Biological Evolution</subject><subject>Cis-regulation</subject><subject>Commentary</subject><subject>DNA</subject><subject>Drosophila</subject><subject>Evolution</subject><subject>evolution of development</subject><subject>Evolutionary biology</subject><subject>Evolutionary genetics</subject><subject>gene regulation</subject><subject>Genes</subject><subject>Genetic mutation</subject><subject>Genetics</subject><subject>Genomics</subject><subject>Morphogenesis - genetics</subject><subject>Mutation</subject><subject>phenotypic evolution</subject><subject>Phenotypic traits</subject><subject>Regulatory Elements, Transcriptional</subject><subject>structural gene</subject><subject>Transcription factors</subject><issn>0014-3820</issn><issn>1558-5646</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkV9r2zAUxUXZaLO232AMs4e92buSdfVnDIqXuGkgxIU4a9-E7ShgL4k7O6Hpt69cdxnsZdWDdNH5HaF7DyEehYC69bUKKKLyUXARMAAZAFDA4HBCBkfhHRm4W-6HisEZ-dC2FQBopPqUnFHJNdMoBuQqvYm9aTJczL3k2ot_JtNFOklm37rSG3VbNBt5HTSOZ3E6Gb5w0Si6TaMOvCDvV9m6tZev5zlZXMfp8MafJuPJMJr6OVKGfqFYFnLBFCByYcVKq1AusVjmBQO6VEWOOXK6YtaqDCUtQuSKU2q1K1Dn4Tn50r_70NS_97bdmU3ZFna9zra23rdGguM5sP-CVGtgKMUbQCUV09qBn_8Bq3rfbF23hjEJrh-uHPTpFdrnG7s0D025yZon82fSDvjeA4_l2j791cF0iZrKdMGZLjjTJWpeEjUH4yJwhbN_7O1Vu6ubo92NlIYITvZ7uWx39nCUs-aXETKUaO5mY3M3_4Ewv703944XPZ-Xdb21b_5O-AxUw7L3</recordid><startdate>200705</startdate><enddate>200705</enddate><creator>Hoekstra, Hopi E.</creator><creator>Coyne, Jerry A.</creator><general>Blackwell Science Inc</general><general>Blackwell Publishing Inc</general><general>Society for the Study of Evolution</general><general>Oxford University Press</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>200705</creationdate><title>THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION</title><author>Hoekstra, Hopi E. ; Coyne, Jerry A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b5125-c82a3462805546e6f9837d5cdbc201d8cb5b541f2ee8a571c3548411e935459b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Animals</topic><topic>Biological adaptation</topic><topic>Biological Evolution</topic><topic>Cis-regulation</topic><topic>Commentary</topic><topic>DNA</topic><topic>Drosophila</topic><topic>Evolution</topic><topic>evolution of development</topic><topic>Evolutionary biology</topic><topic>Evolutionary genetics</topic><topic>gene regulation</topic><topic>Genes</topic><topic>Genetic mutation</topic><topic>Genetics</topic><topic>Genomics</topic><topic>Morphogenesis - genetics</topic><topic>Mutation</topic><topic>phenotypic evolution</topic><topic>Phenotypic traits</topic><topic>Regulatory Elements, Transcriptional</topic><topic>structural gene</topic><topic>Transcription factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hoekstra, Hopi E.</creatorcontrib><creatorcontrib>Coyne, Jerry A.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</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>Neurosciences Abstracts</collection><collection>Nucleic Acids 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>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hoekstra, Hopi E.</au><au>Coyne, Jerry A.</au><au>Rausher, M</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION</atitle><jtitle>Evolution</jtitle><addtitle>Evolution</addtitle><date>2007-05</date><risdate>2007</risdate><volume>61</volume><issue>5</issue><spage>995</spage><epage>1016</epage><pages>995-1016</pages><issn>0014-3820</issn><eissn>1558-5646</eissn><abstract>An important tenet of evolutionary developmental biology (“evo devo”) is that adaptive mutations affecting morphology are more likely to occur in the cis-regulatory regions than in the protein-coding regions of genes. This argument rests on two claims: (1) the modular nature of cis-regulatory elements largely frees them from deleterious pleiotropic effects, and (2) a growing body of empirical evidence appears to support the predominant role of gene regulatory change in adaptation, especially morphological adaptation. Here we discuss and critique these assertions. We first show that there is no theoretical or empirical basis for the evo devo contention that adaptations involving morphology evolve by genetic mechanisms different from those involving physiology and other traits. In addition, some forms of protein evolution can avoid the negative consequences of pleiotropy, most notably via gene duplication. In light of evo devo claims, we then examine the substantial data on the genetic basis of adaptation from both genome-wide surveys and single-locus studies. Genomic studies lend little support to the cis-regulatory theory: many of these have detected adaptation in protein-coding regions, including transcription factors, whereas few have examined regulatory regions. Turning to single-locus studies, we note that the most widely cited examples of adaptive cis-regulatory mutations focus on trait loss rather than gain, and none have yet pinpointed an evolved regulatory site. In contrast, there are many studies that have both identified structural mutations and functionally verified their contribution to adaptation and speciation. Neither the theoretical arguments nor the data from nature, then, support the claim for a predominance of cis-regulatory mutations in evolution. Although this claim may be true, it is at best premature. 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subjects | Animals Biological adaptation Biological Evolution Cis-regulation Commentary DNA Drosophila Evolution evolution of development Evolutionary biology Evolutionary genetics gene regulation Genes Genetic mutation Genetics Genomics Morphogenesis - genetics Mutation phenotypic evolution Phenotypic traits Regulatory Elements, Transcriptional structural gene Transcription factors |
title | THE LOCUS OF EVOLUTION: EVO DEVO AND THE GENETICS OF ADAPTATION |
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