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...
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Veröffentlicht in: | Evolution 2011-08, Vol.65 (8), p.2399-2411 |
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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 |
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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 & 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</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 & development</subject><subject>Evolutionary genetics</subject><subject>Fertilization</subject><subject>Genetic Pleiotropy</subject><subject>Genetic variation</subject><subject>Genetics</subject><subject>Genitalia - anatomy & histology</subject><subject>Genitalia - physiology</subject><subject>Genotype & 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 & histology</subject><subject>Snails - genetics</subject><subject>Snails - physiology</subject><subject>Zygote - growth & 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. 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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 & development</topic><topic>Evolutionary genetics</topic><topic>Fertilization</topic><topic>Genetic Pleiotropy</topic><topic>Genetic variation</topic><topic>Genetics</topic><topic>Genitalia - anatomy & histology</topic><topic>Genitalia - physiology</topic><topic>Genotype & 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 & histology</topic><topic>Snails - genetics</topic><topic>Snails - physiology</topic><topic>Zygote - growth & 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. 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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. 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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 |
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