Loading…

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...

Full description

Saved in:
Bibliographic Details
Published in:BMC evolutionary biology 2013-07, Vol.13 (1), p.153-153
Main Authors: Diepeveen, Eveline T, Kim, Fabienne D, Salzburger, Walter
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3
cites cdi_FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3
container_end_page 153
container_issue 1
container_start_page 153
container_title BMC evolutionary biology
container_volume 13
creator Diepeveen, Eveline T
Kim, Fabienne D
Salzburger, Walter
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.
doi_str_mv 10.1186/1471-2148-13-153
format article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3728225</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3036009781</sourcerecordid><originalsourceid>FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3</originalsourceid><addsrcrecordid>eNpdkU2LFDEQhhtR3A-9e5KAFy-tSeezL8KyrK6w4EE9hyRTmc6STsake9i5-dPtZtZh9ZQi9dZDUk_TvCH4AyFKfCRMkrYjTLWEtoTTZ8356er5k_qsuaj1HmMiVUdeNmcdVYL3XJw3v7_DrxmSA2SSiYcKFWWPpgHQJtTJxDZCrWjII2SbH9AWEiBvxhAPKCR0Y-qErnwJziTkghti2CAf6rBgCuzBRFTDNplpLkfwLtcwhT2gChHcFHJ61bzwJlZ4_XheNj8_3_y4vm3vvn35en111zrG5dQqyzYKSM89ZpRwrywYITm11FnGhPGE2N4YK3HfWcx6J0AIzJV10nLee3rZfDpyd7MdYeMgTcVEvSthNOWgswn6304Kg97mvaayU13HF8D7R0DJy8rqpMdQHcRoEuS5asI6iTElSi7Rd_9F7_Nclv2uKSIZFlKuQHxMuZJrLeBPjyFYr3r16k-v_jShetG7jLx9-onTwF-f9A_8eqKJ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1417406775</pqid></control><display><type>article</type><title>Sequence analyses of the distal-less homeobox gene family in East African cichlid fishes reveal signatures of positive selection</title><source>Publicly Available Content Database</source><source>PubMed Central</source><creator>Diepeveen, Eveline T ; Kim, Fabienne D ; Salzburger, Walter</creator><creatorcontrib>Diepeveen, Eveline T ; Kim, Fabienne D ; Salzburger, Walter</creatorcontrib><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><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 &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Health &amp; 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 &amp; 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 &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; 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 &amp; Fisheries Abstracts (ASFA) 1: Biological Sciences &amp; Living Resources</collection><collection>Aquatic Science &amp; 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>
fulltext fulltext
identifier ISSN: 1471-2148
ispartof BMC evolutionary biology, 2013-07, Vol.13 (1), p.153-153
issn 1471-2148
1471-2148
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3728225
source Publicly Available Content Database; PubMed Central
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
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T22%3A26%3A58IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Sequence%20analyses%20of%20the%20distal-less%20homeobox%20gene%20family%20in%20East%20African%20cichlid%20fishes%20reveal%20signatures%20of%20positive%20selection&rft.jtitle=BMC%20evolutionary%20biology&rft.au=Diepeveen,%20Eveline%20T&rft.date=2013-07-17&rft.volume=13&rft.issue=1&rft.spage=153&rft.epage=153&rft.pages=153-153&rft.issn=1471-2148&rft.eissn=1471-2148&rft_id=info:doi/10.1186/1471-2148-13-153&rft_dat=%3Cproquest_pubme%3E3036009781%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c457t-8b4d8e195f04315f8bea6753b3cb446af11b9aab7092b049c6e66058bc7b559f3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1417406775&rft_id=info:pmid/23865956&rfr_iscdi=true