The Diversity and Evolution of Sex Chromosomes in Frogs
Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distr...
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Veröffentlicht in: | Genes 2021-03, Vol.12 (4), p.483 |
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description | Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems. |
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We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.</description><identifier>ISSN: 2073-4425</identifier><identifier>EISSN: 2073-4425</identifier><identifier>DOI: 10.3390/genes12040483</identifier><identifier>PMID: 33810524</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Animal behavior ; Animals ; Anura - classification ; Anura - genetics ; Binding sites ; Divergence ; Evolution ; Evolution, Molecular ; Female ; Females ; Frogs ; Genes ; Genomes ; Haplotypes ; Male ; Males ; Mutation ; Ovaries ; Phylogeny ; Recombination ; Review ; Sex chromosomes ; Sex Chromosomes - genetics ; Sex determination ; Sex Determination Processes ; Sexual selection ; Telomeres</subject><ispartof>Genes, 2021-03, Vol.12 (4), p.483</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 by the authors. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c481t-b02a4a87fe0040dc57fe47ca669e9b7005de7bb4210a3b299d65b3cd1326e183</citedby><cites>FETCH-LOGICAL-c481t-b02a4a87fe0040dc57fe47ca669e9b7005de7bb4210a3b299d65b3cd1326e183</cites><orcidid>0000-0003-2585-6406 ; 0000-0002-8872-6281</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8067296/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8067296/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33810524$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ma, Wen-Juan</creatorcontrib><creatorcontrib>Veltsos, Paris</creatorcontrib><title>The Diversity and Evolution of Sex Chromosomes in Frogs</title><title>Genes</title><addtitle>Genes (Basel)</addtitle><description>Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.</description><subject>Animal behavior</subject><subject>Animals</subject><subject>Anura - classification</subject><subject>Anura - genetics</subject><subject>Binding sites</subject><subject>Divergence</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Female</subject><subject>Females</subject><subject>Frogs</subject><subject>Genes</subject><subject>Genomes</subject><subject>Haplotypes</subject><subject>Male</subject><subject>Males</subject><subject>Mutation</subject><subject>Ovaries</subject><subject>Phylogeny</subject><subject>Recombination</subject><subject>Review</subject><subject>Sex chromosomes</subject><subject>Sex Chromosomes - genetics</subject><subject>Sex determination</subject><subject>Sex Determination Processes</subject><subject>Sexual selection</subject><subject>Telomeres</subject><issn>2073-4425</issn><issn>2073-4425</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNpdkc1Lw0AQxRdRbKk9epUFL16i-5lsLoLUVoWCB3tfNsm03ZJk625S7H9vSmtpncsMzI83b3gI3VLyyHlKnhZQQ6CMCCIUv0B9RhIeCcHk5cncQ8MQVqQrQRgh8hr1OFeUSCb6KJktAb_aDfhgmy02dYHHG1e2jXU1dnP8BT94tPSucsFVELCt8cS7RbhBV3NTBhge-gDNJuPZ6D2afr59jF6mUS4UbaKMMCOMSuawu17ksptEkps4TiHNks5NAUmWCUaJ4RlL0yKWGc8LylkMVPEBet7LrtusgiKHuvGm1GtvK-O32hmrzze1XeqF22hF4oSlcSfwcBDw7ruF0OjKhhzK0tTg2qCZJErGIlG7W_f_0JVrfd1911GccqWIlB0V7ancuxA8zI9mKNG7UPRZKB1_d_rBkf6LgP8Ct_KHOQ</recordid><startdate>20210326</startdate><enddate>20210326</enddate><creator>Ma, Wen-Juan</creator><creator>Veltsos, Paris</creator><general>MDPI AG</general><general>MDPI</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>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-2585-6406</orcidid><orcidid>https://orcid.org/0000-0002-8872-6281</orcidid></search><sort><creationdate>20210326</creationdate><title>The Diversity and Evolution of Sex Chromosomes in Frogs</title><author>Ma, Wen-Juan ; Veltsos, Paris</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c481t-b02a4a87fe0040dc57fe47ca669e9b7005de7bb4210a3b299d65b3cd1326e183</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Animal behavior</topic><topic>Animals</topic><topic>Anura - classification</topic><topic>Anura - genetics</topic><topic>Binding sites</topic><topic>Divergence</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Female</topic><topic>Females</topic><topic>Frogs</topic><topic>Genes</topic><topic>Genomes</topic><topic>Haplotypes</topic><topic>Male</topic><topic>Males</topic><topic>Mutation</topic><topic>Ovaries</topic><topic>Phylogeny</topic><topic>Recombination</topic><topic>Review</topic><topic>Sex chromosomes</topic><topic>Sex Chromosomes - genetics</topic><topic>Sex determination</topic><topic>Sex Determination Processes</topic><topic>Sexual selection</topic><topic>Telomeres</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ma, Wen-Juan</creatorcontrib><creatorcontrib>Veltsos, Paris</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Genes</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ma, Wen-Juan</au><au>Veltsos, Paris</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Diversity and Evolution of Sex Chromosomes in Frogs</atitle><jtitle>Genes</jtitle><addtitle>Genes (Basel)</addtitle><date>2021-03-26</date><risdate>2021</risdate><volume>12</volume><issue>4</issue><spage>483</spage><pages>483-</pages><issn>2073-4425</issn><eissn>2073-4425</eissn><abstract>Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>33810524</pmid><doi>10.3390/genes12040483</doi><orcidid>https://orcid.org/0000-0003-2585-6406</orcidid><orcidid>https://orcid.org/0000-0002-8872-6281</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animal behavior Animals Anura - classification Anura - genetics Binding sites Divergence Evolution Evolution, Molecular Female Females Frogs Genes Genomes Haplotypes Male Males Mutation Ovaries Phylogeny Recombination Review Sex chromosomes Sex Chromosomes - genetics Sex determination Sex Determination Processes Sexual selection Telomeres |
title | The Diversity and Evolution of Sex Chromosomes in Frogs |
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