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Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection
Gen(om)e duplication events are hypothesized as key mechanisms underlying the origin of phenotypic diversity and evolutionary innovation. The diverse and species-rich lineage of teleost fishes is a renowned example of this scenario, because of the fish-specific genome duplication. Gene families, gen...
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Published in: | BMC evolutionary biology 2013-07, Vol.13 (1), p.153-153 |
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description | Gen(om)e duplication events are hypothesized as key mechanisms underlying the origin of phenotypic diversity and evolutionary innovation. The diverse and species-rich lineage of teleost fishes is a renowned example of this scenario, because of the fish-specific genome duplication. Gene families, generated by this and other gene duplication events, have been previously found to play a role in the evolution and development of innovations in cichlid fishes - a prime model system to study the genetic basis of rapid speciation, adaptation and evolutionary innovation. The distal-less homeobox genes are particularly interesting candidate genes for evolutionary novelties, such as the pharyngeal jaw apparatus and the anal fin egg-spots. Here we study the dlx repertoire in 23 East African cichlid fishes to determine the rate of evolution and the signatures of selection pressure.
Four intact dlx clusters were retrieved from cichlid draft genomes. Phylogenetic analyses of these eight dlx loci in ten teleost species, followed by an in-depth analysis of 23 East African cichlid species, show that there is disparity in the rates of evolution of the dlx paralogs. Dlx3a and dlx4b are the fastest evolving dlx genes, while dlx1a and dlx6a evolved more slowly. Subsequent analyses of the nonsynonymous-synonymous substitution rate ratios indicate that dlx3b, dlx4a and dlx5a evolved under purifying selection, while signs of positive selection were found for dlx1a, dlx2a, dlx3a and dlx4b.
Our results indicate that the dlx repertoire of teleost fishes and cichlid fishes in particular, is shaped by differential selection pressures and rates of evolution after gene duplication. Although the divergence of the dlx paralogs are putative signs of new or altered functions, comparisons with available expression patterns indicate that the three dlx loci under strong purifying selection, dlx3b, dlx4a and dlx5a, are transcribed at high levels in the cichlids' pharyngeal jaw and anal fin. The dlx paralogs emerge as excellent candidate genes for the development of evolutionary innovations in cichlids, although further functional analyses are necessary to elucidate their respective contribution. |
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Four intact dlx clusters were retrieved from cichlid draft genomes. Phylogenetic analyses of these eight dlx loci in ten teleost species, followed by an in-depth analysis of 23 East African cichlid species, show that there is disparity in the rates of evolution of the dlx paralogs. Dlx3a and dlx4b are the fastest evolving dlx genes, while dlx1a and dlx6a evolved more slowly. Subsequent analyses of the nonsynonymous-synonymous substitution rate ratios indicate that dlx3b, dlx4a and dlx5a evolved under purifying selection, while signs of positive selection were found for dlx1a, dlx2a, dlx3a and dlx4b.
Our results indicate that the dlx repertoire of teleost fishes and cichlid fishes in particular, is shaped by differential selection pressures and rates of evolution after gene duplication. Although the divergence of the dlx paralogs are putative signs of new or altered functions, comparisons with available expression patterns indicate that the three dlx loci under strong purifying selection, dlx3b, dlx4a and dlx5a, are transcribed at high levels in the cichlids' pharyngeal jaw and anal fin. The dlx paralogs emerge as excellent candidate genes for the development of evolutionary innovations in cichlids, although further functional analyses are necessary to elucidate their respective contribution.</description><identifier>ISSN: 1471-2148</identifier><identifier>EISSN: 1471-2148</identifier><identifier>DOI: 10.1186/1471-2148-13-153</identifier><identifier>PMID: 23865956</identifier><language>eng</language><publisher>England: BioMed Central</publisher><subject>Amino Acid Sequence ; Animals ; Cichlidae ; Cichlids - classification ; Cichlids - genetics ; Evolution ; Evolution, Molecular ; Fish Proteins - chemistry ; Fish Proteins - genetics ; Fishes - classification ; Fishes - genetics ; Freshwater ; Gene Duplication ; Genes ; Genome ; Genomes ; Homeodomain Proteins - chemistry ; Homeodomain Proteins - genetics ; Molecular Sequence Data ; Multigene Family ; Phylogenetics ; Phylogeny ; Pisces ; Proteins ; Selection, Genetic ; Sequence Alignment ; Teleostei ; Vertebrates ; Zebrafish</subject><ispartof>BMC evolutionary biology, 2013-07, Vol.13 (1), p.153-153</ispartof><rights>2013 Diepeveen et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</rights><rights>Copyright © 2013 Diepeveen et al.; licensee BioMed Central Ltd. 2013 Diepeveen et al.; licensee BioMed Central Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3</citedby><cites>FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3</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/PMC3728225/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1417406775?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23865956$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Diepeveen, Eveline T</creatorcontrib><creatorcontrib>Kim, Fabienne D</creatorcontrib><creatorcontrib>Salzburger, Walter</creatorcontrib><title>Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection</title><title>BMC evolutionary biology</title><addtitle>BMC Evol Biol</addtitle><description>Gen(om)e duplication events are hypothesized as key mechanisms underlying the origin of phenotypic diversity and evolutionary innovation. The diverse and species-rich lineage of teleost fishes is a renowned example of this scenario, because of the fish-specific genome duplication. Gene families, generated by this and other gene duplication events, have been previously found to play a role in the evolution and development of innovations in cichlid fishes - a prime model system to study the genetic basis of rapid speciation, adaptation and evolutionary innovation. The distal-less homeobox genes are particularly interesting candidate genes for evolutionary novelties, such as the pharyngeal jaw apparatus and the anal fin egg-spots. Here we study the dlx repertoire in 23 East African cichlid fishes to determine the rate of evolution and the signatures of selection pressure.
Four intact dlx clusters were retrieved from cichlid draft genomes. Phylogenetic analyses of these eight dlx loci in ten teleost species, followed by an in-depth analysis of 23 East African cichlid species, show that there is disparity in the rates of evolution of the dlx paralogs. Dlx3a and dlx4b are the fastest evolving dlx genes, while dlx1a and dlx6a evolved more slowly. Subsequent analyses of the nonsynonymous-synonymous substitution rate ratios indicate that dlx3b, dlx4a and dlx5a evolved under purifying selection, while signs of positive selection were found for dlx1a, dlx2a, dlx3a and dlx4b.
Our results indicate that the dlx repertoire of teleost fishes and cichlid fishes in particular, is shaped by differential selection pressures and rates of evolution after gene duplication. Although the divergence of the dlx paralogs are putative signs of new or altered functions, comparisons with available expression patterns indicate that the three dlx loci under strong purifying selection, dlx3b, dlx4a and dlx5a, are transcribed at high levels in the cichlids' pharyngeal jaw and anal fin. The dlx paralogs emerge as excellent candidate genes for the development of evolutionary innovations in cichlids, although further functional analyses are necessary to elucidate their respective contribution.</description><subject>Amino Acid Sequence</subject><subject>Animals</subject><subject>Cichlidae</subject><subject>Cichlids - classification</subject><subject>Cichlids - genetics</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Fish Proteins - chemistry</subject><subject>Fish Proteins - genetics</subject><subject>Fishes - classification</subject><subject>Fishes - genetics</subject><subject>Freshwater</subject><subject>Gene Duplication</subject><subject>Genes</subject><subject>Genome</subject><subject>Genomes</subject><subject>Homeodomain Proteins - chemistry</subject><subject>Homeodomain Proteins - genetics</subject><subject>Molecular Sequence Data</subject><subject>Multigene Family</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Pisces</subject><subject>Proteins</subject><subject>Selection, Genetic</subject><subject>Sequence Alignment</subject><subject>Teleostei</subject><subject>Vertebrates</subject><subject>Zebrafish</subject><issn>1471-2148</issn><issn>1471-2148</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNpdkU2LFDEQhhtR3A-9e5KAFy-tSeezL8KyrK6w4EE9hyRTmc6STsake9i5-dPtZtZh9ZQi9dZDUk_TvCH4AyFKfCRMkrYjTLWEtoTTZ8356er5k_qsuaj1HmMiVUdeNmcdVYL3XJw3v7_DrxmSA2SSiYcKFWWPpgHQJtTJxDZCrWjII2SbH9AWEiBvxhAPKCR0Y-qErnwJziTkghti2CAf6rBgCuzBRFTDNplpLkfwLtcwhT2gChHcFHJ61bzwJlZ4_XheNj8_3_y4vm3vvn35en111zrG5dQqyzYKSM89ZpRwrywYITm11FnGhPGE2N4YK3HfWcx6J0AIzJV10nLee3rZfDpyd7MdYeMgTcVEvSthNOWgswn6304Kg97mvaayU13HF8D7R0DJy8rqpMdQHcRoEuS5asI6iTElSi7Rd_9F7_Nclv2uKSIZFlKuQHxMuZJrLeBPjyFYr3r16k-v_jShetG7jLx9-onTwF-f9A_8eqKJ</recordid><startdate>20130717</startdate><enddate>20130717</enddate><creator>Diepeveen, Eveline T</creator><creator>Kim, Fabienne D</creator><creator>Salzburger, Walter</creator><general>BioMed Central</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>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope></search><sort><creationdate>20130717</creationdate><title>Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection</title><author>Diepeveen, Eveline T ; Kim, Fabienne D ; Salzburger, Walter</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Amino Acid Sequence</topic><topic>Animals</topic><topic>Cichlidae</topic><topic>Cichlids - classification</topic><topic>Cichlids - genetics</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Fish Proteins - chemistry</topic><topic>Fish Proteins - genetics</topic><topic>Fishes - classification</topic><topic>Fishes - genetics</topic><topic>Freshwater</topic><topic>Gene Duplication</topic><topic>Genes</topic><topic>Genome</topic><topic>Genomes</topic><topic>Homeodomain Proteins - chemistry</topic><topic>Homeodomain Proteins - genetics</topic><topic>Molecular Sequence Data</topic><topic>Multigene Family</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Pisces</topic><topic>Proteins</topic><topic>Selection, Genetic</topic><topic>Sequence Alignment</topic><topic>Teleostei</topic><topic>Vertebrates</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Diepeveen, Eveline T</creatorcontrib><creatorcontrib>Kim, Fabienne D</creatorcontrib><creatorcontrib>Salzburger, Walter</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</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>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>BMC evolutionary biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Diepeveen, Eveline T</au><au>Kim, Fabienne D</au><au>Salzburger, Walter</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection</atitle><jtitle>BMC evolutionary biology</jtitle><addtitle>BMC Evol Biol</addtitle><date>2013-07-17</date><risdate>2013</risdate><volume>13</volume><issue>1</issue><spage>153</spage><epage>153</epage><pages>153-153</pages><issn>1471-2148</issn><eissn>1471-2148</eissn><abstract>Gen(om)e duplication events are hypothesized as key mechanisms underlying the origin of phenotypic diversity and evolutionary innovation. The diverse and species-rich lineage of teleost fishes is a renowned example of this scenario, because of the fish-specific genome duplication. Gene families, generated by this and other gene duplication events, have been previously found to play a role in the evolution and development of innovations in cichlid fishes - a prime model system to study the genetic basis of rapid speciation, adaptation and evolutionary innovation. The distal-less homeobox genes are particularly interesting candidate genes for evolutionary novelties, such as the pharyngeal jaw apparatus and the anal fin egg-spots. Here we study the dlx repertoire in 23 East African cichlid fishes to determine the rate of evolution and the signatures of selection pressure.
Four intact dlx clusters were retrieved from cichlid draft genomes. Phylogenetic analyses of these eight dlx loci in ten teleost species, followed by an in-depth analysis of 23 East African cichlid species, show that there is disparity in the rates of evolution of the dlx paralogs. Dlx3a and dlx4b are the fastest evolving dlx genes, while dlx1a and dlx6a evolved more slowly. Subsequent analyses of the nonsynonymous-synonymous substitution rate ratios indicate that dlx3b, dlx4a and dlx5a evolved under purifying selection, while signs of positive selection were found for dlx1a, dlx2a, dlx3a and dlx4b.
Our results indicate that the dlx repertoire of teleost fishes and cichlid fishes in particular, is shaped by differential selection pressures and rates of evolution after gene duplication. Although the divergence of the dlx paralogs are putative signs of new or altered functions, comparisons with available expression patterns indicate that the three dlx loci under strong purifying selection, dlx3b, dlx4a and dlx5a, are transcribed at high levels in the cichlids' pharyngeal jaw and anal fin. The dlx paralogs emerge as excellent candidate genes for the development of evolutionary innovations in cichlids, although further functional analyses are necessary to elucidate their respective contribution.</abstract><cop>England</cop><pub>BioMed Central</pub><pmid>23865956</pmid><doi>10.1186/1471-2148-13-153</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Animals Cichlidae Cichlids - classification Cichlids - genetics Evolution Evolution, Molecular Fish Proteins - chemistry Fish Proteins - genetics Fishes - classification Fishes - genetics Freshwater Gene Duplication Genes Genome Genomes Homeodomain Proteins - chemistry Homeodomain Proteins - genetics Molecular Sequence Data Multigene Family Phylogenetics Phylogeny Pisces Proteins Selection, Genetic Sequence Alignment Teleostei Vertebrates Zebrafish |
title | Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection |
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