INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL

Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia locate...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Evolution 2011-08, Vol.65 (8), p.2399-2411
Hauptverfasser: Utsuno, Hiroki, Asami, Takahiro, Van Dooren, Tom J. M., Gittenberger, Edmund
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 2411
container_issue 8
container_start_page 2399
container_title Evolution
container_volume 65
creator Utsuno, Hiroki
Asami, Takahiro
Van Dooren, Tom J. M.
Gittenberger, Edmund
description Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood. Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistrai snails that share the same zygotic genotype. Before hatching, these sinistrais developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrais. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.
doi_str_mv 10.1111/j.1558-5646.2011.01293.x
format Article
fullrecord <record><control><sourceid>jstor_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_888338957</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>41240829</jstor_id><sourcerecordid>41240829</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4723-311251197f9dd1e37e0bdb618d036fb98e8ce88fd184b2cac73493164c106cf83</originalsourceid><addsrcrecordid>eNpdkV9PwjAUxRujUUQ_gmbxxafN3nVd2wdjFiywZBkRJvrW7E-XMEFwg4jf3g6QB_vSpud3bm7OQcgC7IA5D5UDlHKb-p7vuBjAweAK4mxPUOconKIOxuDZhLv4Al02TYUxFhTEObpwgQlMOe2gpzBO5DgOImsiI9lLwlFsBYMgjCeJlQylJaej6HX3O-pbkewn9jgcDBNrLKdyPAmiK3RWpvNGXx_uLnrty6Q3tKPRIOwFkZ17zCU2AXApgGClKArQhGmcFZkPvMDELzPBNc8152UB3MvcPM0Z8QQB38sB-3nJSRfd7-eu6uXXRjdrtZg1uZ7P00-93DSKc04IF5QZ8u4fWS039adZzkBEADNTDXR7gDbZQhdqVc8Waf2j_oIxwOMe-J7N9c9RB6zaAlSl2pxVm7NqC1C7AtRWmbzal_Hf7P1Vs17WR78Hroe5AbrI3uuzZq23Rz2tP5TPCKPqLR6oKaHP8Pz-ol7IL6gViaA</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>883917164</pqid></control><display><type>article</type><title>INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL</title><source>MEDLINE</source><source>Access via Wiley Online Library</source><source>JSTOR Archive Collection A-Z Listing</source><source>Oxford University Press Journals All Titles (1996-Current)</source><source>EZB-FREE-00999 freely available EZB journals</source><creator>Utsuno, Hiroki ; Asami, Takahiro ; Van Dooren, Tom J. M. ; Gittenberger, Edmund</creator><creatorcontrib>Utsuno, Hiroki ; Asami, Takahiro ; Van Dooren, Tom J. M. ; Gittenberger, Edmund</creatorcontrib><description>Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood. Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistrai snails that share the same zygotic genotype. Before hatching, these sinistrais developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrais. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.</description><identifier>ISSN: 0014-3820</identifier><identifier>EISSN: 1558-5646</identifier><identifier>DOI: 10.1111/j.1558-5646.2011.01293.x</identifier><identifier>PMID: 21790585</identifier><language>eng</language><publisher>Malden, USA: Blackwell Publishing Inc</publisher><subject>Animals ; Biological Evolution ; Centroids ; Chirality ; Embryos ; Enantiomers ; Epistasis, Genetic ; Evolution ; Evolution &amp; development ; Evolutionary genetics ; Fertilization ; Genetic Pleiotropy ; Genetic variation ; Genetics ; Genitalia - anatomy &amp; histology ; Genitalia - physiology ; Genotype &amp; phenotype ; Genotypes ; homochirality ; maternal epistasis ; maternal inheritance ; maternal pleiotropy ; Mollusks ; Morphology ; Phenotype ; Phenotypes ; Phenotypic traits ; Selection, Genetic ; situs inversus ; Snails ; Snails - anatomy &amp; histology ; Snails - genetics ; Snails - physiology ; Zygote - growth &amp; development ; Zygote - metabolism</subject><ispartof>Evolution, 2011-08, Vol.65 (8), p.2399-2411</ispartof><rights>Copyright © 2011 Society for the Study of Evolution</rights><rights>2011 The Author(s). © 2011 The Society for the Study of Evolution.</rights><rights>2011 The Author(s). Evolution© 2011 The Society for the Study of Evolution.</rights><rights>Copyright Society for the Study of Evolution Aug 2011</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4723-311251197f9dd1e37e0bdb618d036fb98e8ce88fd184b2cac73493164c106cf83</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41240829$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41240829$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>315,782,786,805,1419,27931,27932,45581,45582,58024,58257</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21790585$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Utsuno, Hiroki</creatorcontrib><creatorcontrib>Asami, Takahiro</creatorcontrib><creatorcontrib>Van Dooren, Tom J. M.</creatorcontrib><creatorcontrib>Gittenberger, Edmund</creatorcontrib><title>INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL</title><title>Evolution</title><addtitle>Evolution</addtitle><description>Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood. Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistrai snails that share the same zygotic genotype. Before hatching, these sinistrais developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrais. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.</description><subject>Animals</subject><subject>Biological Evolution</subject><subject>Centroids</subject><subject>Chirality</subject><subject>Embryos</subject><subject>Enantiomers</subject><subject>Epistasis, Genetic</subject><subject>Evolution</subject><subject>Evolution &amp; development</subject><subject>Evolutionary genetics</subject><subject>Fertilization</subject><subject>Genetic Pleiotropy</subject><subject>Genetic variation</subject><subject>Genetics</subject><subject>Genitalia - anatomy &amp; histology</subject><subject>Genitalia - physiology</subject><subject>Genotype &amp; phenotype</subject><subject>Genotypes</subject><subject>homochirality</subject><subject>maternal epistasis</subject><subject>maternal inheritance</subject><subject>maternal pleiotropy</subject><subject>Mollusks</subject><subject>Morphology</subject><subject>Phenotype</subject><subject>Phenotypes</subject><subject>Phenotypic traits</subject><subject>Selection, Genetic</subject><subject>situs inversus</subject><subject>Snails</subject><subject>Snails - anatomy &amp; histology</subject><subject>Snails - genetics</subject><subject>Snails - physiology</subject><subject>Zygote - growth &amp; development</subject><subject>Zygote - metabolism</subject><issn>0014-3820</issn><issn>1558-5646</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV9PwjAUxRujUUQ_gmbxxafN3nVd2wdjFiywZBkRJvrW7E-XMEFwg4jf3g6QB_vSpud3bm7OQcgC7IA5D5UDlHKb-p7vuBjAweAK4mxPUOconKIOxuDZhLv4Al02TYUxFhTEObpwgQlMOe2gpzBO5DgOImsiI9lLwlFsBYMgjCeJlQylJaej6HX3O-pbkewn9jgcDBNrLKdyPAmiK3RWpvNGXx_uLnrty6Q3tKPRIOwFkZ17zCU2AXApgGClKArQhGmcFZkPvMDELzPBNc8152UB3MvcPM0Z8QQB38sB-3nJSRfd7-eu6uXXRjdrtZg1uZ7P00-93DSKc04IF5QZ8u4fWS039adZzkBEADNTDXR7gDbZQhdqVc8Waf2j_oIxwOMe-J7N9c9RB6zaAlSl2pxVm7NqC1C7AtRWmbzal_Hf7P1Vs17WR78Hroe5AbrI3uuzZq23Rz2tP5TPCKPqLR6oKaHP8Pz-ol7IL6gViaA</recordid><startdate>201108</startdate><enddate>201108</enddate><creator>Utsuno, Hiroki</creator><creator>Asami, Takahiro</creator><creator>Van Dooren, Tom J. M.</creator><creator>Gittenberger, Edmund</creator><general>Blackwell Publishing Inc</general><general>Wiley Subscription Services, Inc</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>201108</creationdate><title>INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL</title><author>Utsuno, Hiroki ; Asami, Takahiro ; Van Dooren, Tom J. M. ; Gittenberger, Edmund</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4723-311251197f9dd1e37e0bdb618d036fb98e8ce88fd184b2cac73493164c106cf83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Biological Evolution</topic><topic>Centroids</topic><topic>Chirality</topic><topic>Embryos</topic><topic>Enantiomers</topic><topic>Epistasis, Genetic</topic><topic>Evolution</topic><topic>Evolution &amp; development</topic><topic>Evolutionary genetics</topic><topic>Fertilization</topic><topic>Genetic Pleiotropy</topic><topic>Genetic variation</topic><topic>Genetics</topic><topic>Genitalia - anatomy &amp; histology</topic><topic>Genitalia - physiology</topic><topic>Genotype &amp; phenotype</topic><topic>Genotypes</topic><topic>homochirality</topic><topic>maternal epistasis</topic><topic>maternal inheritance</topic><topic>maternal pleiotropy</topic><topic>Mollusks</topic><topic>Morphology</topic><topic>Phenotype</topic><topic>Phenotypes</topic><topic>Phenotypic traits</topic><topic>Selection, Genetic</topic><topic>situs inversus</topic><topic>Snails</topic><topic>Snails - anatomy &amp; histology</topic><topic>Snails - genetics</topic><topic>Snails - physiology</topic><topic>Zygote - growth &amp; development</topic><topic>Zygote - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Utsuno, Hiroki</creatorcontrib><creatorcontrib>Asami, Takahiro</creatorcontrib><creatorcontrib>Van Dooren, Tom J. M.</creatorcontrib><creatorcontrib>Gittenberger, Edmund</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 &amp; 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>Utsuno, Hiroki</au><au>Asami, Takahiro</au><au>Van Dooren, Tom J. M.</au><au>Gittenberger, Edmund</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL</atitle><jtitle>Evolution</jtitle><addtitle>Evolution</addtitle><date>2011-08</date><risdate>2011</risdate><volume>65</volume><issue>8</issue><spage>2399</spage><epage>2411</epage><pages>2399-2411</pages><issn>0014-3820</issn><eissn>1558-5646</eissn><abstract>Among metazoan species, left-right reversals in primary asymmetry have rarely gone to fixation. This suggests that a general mechanism suppresses the evolution of polarity reversal. Most metazoans appear externally symmetric and reproduce by external fertilization or copulation with genitalia located in the midline. Thus, reversal should generate little exogenous disadvantage when interacting with the external environment or in mating with the common wild-type. Accordingly, an endogenously caused fitness reduction may be responsible for the general absence of reversed species. However, how this selection operates is little understood. Phenotypic changes associated with reversal are usually inseparable from zygotic pleiotropy. By exploiting hermaphroditism and the maternal inheritance of left-right polarity, we generated dextral and sinistrai snails that share the same zygotic genotype. Before hatching, these sinistrais developed lethal morphological anomalies more frequently than dextrals. Their shell shape at maturity differed from the mirror image of the dextral shell. These interchiral differences demonstrate pleiotropy in maternal effects of the polarity or linked genes. Variation in interchiral differences between parental crosses suggests the presence of epistatic variation in relative performance of sinistrais. Our results show that internal selection operates against polarity reversal, and we suggest that this is due to changes in blastomere configuration.</abstract><cop>Malden, USA</cop><pub>Blackwell Publishing Inc</pub><pmid>21790585</pmid><doi>10.1111/j.1558-5646.2011.01293.x</doi><tpages>13</tpages></addata></record>
fulltext fulltext
identifier ISSN: 0014-3820
ispartof Evolution, 2011-08, Vol.65 (8), p.2399-2411
issn 0014-3820
1558-5646
language eng
recordid cdi_proquest_miscellaneous_888338957
source MEDLINE; Access via Wiley Online Library; JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals
subjects Animals
Biological Evolution
Centroids
Chirality
Embryos
Enantiomers
Epistasis, Genetic
Evolution
Evolution & development
Evolutionary genetics
Fertilization
Genetic Pleiotropy
Genetic variation
Genetics
Genitalia - anatomy & histology
Genitalia - physiology
Genotype & phenotype
Genotypes
homochirality
maternal epistasis
maternal inheritance
maternal pleiotropy
Mollusks
Morphology
Phenotype
Phenotypes
Phenotypic traits
Selection, Genetic
situs inversus
Snails
Snails - anatomy & histology
Snails - genetics
Snails - physiology
Zygote - growth & development
Zygote - metabolism
title INTERNAL SELECTION AGAINST THE EVOLUTION OF LEFT-RIGHT REVERSAL
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-05T12%3A57%3A44IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=INTERNAL%20SELECTION%20AGAINST%20THE%20EVOLUTION%20OF%20LEFT-RIGHT%20REVERSAL&rft.jtitle=Evolution&rft.au=Utsuno,%20Hiroki&rft.date=2011-08&rft.volume=65&rft.issue=8&rft.spage=2399&rft.epage=2411&rft.pages=2399-2411&rft.issn=0014-3820&rft.eissn=1558-5646&rft_id=info:doi/10.1111/j.1558-5646.2011.01293.x&rft_dat=%3Cjstor_proqu%3E41240829%3C/jstor_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=883917164&rft_id=info:pmid/21790585&rft_jstor_id=41240829&rfr_iscdi=true