Genome duplication in amphibians and fish: an extended synthesis
Identifieur interne : 001390 ( Istex/Corpus ); précédent : 001389; suivant : 001391Genome duplication in amphibians and fish: an extended synthesis
Auteurs : B. K. Mable ; M. A. Alexandrou ; M. I. TaylorSource :
- Journal of Zoology [ 0952-8369 ] ; 2011-07.
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Abstract
Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.
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DOI: 10.1111/j.1469-7998.2011.00829.x
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K." last="Mable">B. K. Mable</name><affiliation><mods:affiliation>Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK</mods:affiliation></affiliation></author><author><name sortKey="Alexandrou, M A" sort="Alexandrou, M A" uniqKey="Alexandrou M" first="M. A." last="Alexandrou">M. A. Alexandrou</name><affiliation><mods:affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</mods:affiliation></affiliation></author><author><name sortKey="Taylor, M I" sort="Taylor, M I" uniqKey="Taylor M" first="M. I." last="Taylor">M. I. Taylor</name><affiliation><mods:affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</mods:affiliation></affiliation></author></analytic><monogr></monogr><series><title level="j">Journal of Zoology</title><idno type="ISSN">0952-8369</idno><idno type="eISSN">1469-7998</idno><imprint><publisher>Blackwell Publishing Ltd</publisher><pubPlace>Oxford, UK</pubPlace><date type="published" when="2011-07">2011-07</date><biblScope unit="volume">284</biblScope><biblScope unit="issue">3</biblScope><biblScope unit="page" from="151">151</biblScope><biblScope unit="page" to="182">182</biblScope></imprint><idno type="ISSN">0952-8369</idno></series><idno type="istex">54AD7647C7FAB81066FC7E45E4EA0ACE71B0B3A7</idno><idno type="DOI">10.1111/j.1469-7998.2011.00829.x</idno><idno type="ArticleID">JZO829</idno></biblStruct></sourceDesc><seriesStmt><idno type="ISSN">0952-8369</idno></seriesStmt></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>amphibians</term><term>climate change</term><term>cytogenetics</term><term>fish</term><term>genome size</term><term>phylogeny</term><term>polyploidy</term><term>unreduced gamete formation</term></keywords></textClass><langUsage><language ident="en">en</language></langUsage></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.</div></front></TEI><istex><corpusName>wiley</corpusName><author><json:item><name>B. K. Mable</name><affiliations><json:string>Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK</json:string></affiliations></json:item><json:item><name>M. A. 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(4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. 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Journal of Zoology © 2011 The Zoological Society of London</p></availability><date>2011</date></publicationStmt><sourceDesc><biblStruct type="inbook"><analytic><title level="a" type="main" xml:lang="en">Genome duplication in amphibians and fish: an extended synthesis</title><author xml:id="author-1"><persName><forename type="first">B. K.</forename><surname>Mable</surname></persName><affiliation>Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK</affiliation></author><author xml:id="author-2"><persName><forename type="first">M. A.</forename><surname>Alexandrou</surname></persName><affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</affiliation></author><author xml:id="author-3"><persName><forename type="first">M. I.</forename><surname>Taylor</surname></persName><affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</affiliation></author></analytic><monogr><title level="j">Journal of Zoology</title><idno type="pISSN">0952-8369</idno><idno type="eISSN">1469-7998</idno><idno type="DOI">10.1111/(ISSN)1469-7998</idno><imprint><publisher>Blackwell Publishing Ltd</publisher><pubPlace>Oxford, UK</pubPlace><date type="published" when="2011-07"></date><biblScope unit="volume">284</biblScope><biblScope unit="issue">3</biblScope><biblScope unit="page" from="151">151</biblScope><biblScope unit="page" to="182">182</biblScope></imprint></monogr><idno type="istex">54AD7647C7FAB81066FC7E45E4EA0ACE71B0B3A7</idno><idno type="DOI">10.1111/j.1469-7998.2011.00829.x</idno><idno type="ArticleID">JZO829</idno></biblStruct></sourceDesc></fileDesc><profileDesc><creation><date>2011</date></creation><langUsage><language ident="en">en</language></langUsage><abstract xml:lang="en"><p>Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. 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Journal of Zoology © 2011 The Zoological Society of London</copyright><eventGroup><event type="xmlConverted" agent="Converter:BPG_TO_WML3G version:2.5.2 mode:FullText" date="2011-06-23"></event><event type="publishedOnlineEarlyUnpaginated" date="2011-06-21"></event><event type="firstOnline" date="2011-06-21"></event><event type="publishedOnlineFinalForm" date="2011-06-23"></event><event type="xmlConverted" agent="Converter:WILEY_ML3G_TO_WILEY_ML3GV2 version:3.8.8" date="2014-02-01"></event><event type="xmlConverted" agent="Converter:WML3G_To_WML3G version:4.1.7 mode:FullText,remove_FC" date="2014-10-31"></event></eventGroup><numberingGroup><numbering type="pageFirst" number="151">151</numbering><numbering type="pageLast" number="182">182</numbering></numberingGroup><correspondenceTo><b>Correspondence</b>
Barbara K. Mable, Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow G12 8QQ, UK.
Email: <email normalForm="barbara.mable@glasgow.ac.uk">barbara.mable@glasgow.ac.uk</email></correspondenceTo><linkGroup><link type="toTypesetVersion" href="file:JZO.JZO829.pdf"></link></linkGroup></publicationMeta><contentMeta><unparsedEditorialHistory>Received 10 September 2010; revised 23 February 2011; accepted 25 April 2011</unparsedEditorialHistory><countGroup><count type="figureTotal" number="4"></count><count type="tableTotal" number="2"></count><count type="formulaTotal" number="0"></count><count type="referenceTotal" number="353"></count><count type="wordTotal" number="31420"></count><count type="linksCrossRef" number="318"></count></countGroup><titleGroup><title type="main">Genome duplication in amphibians and fish: an extended synthesis</title><title type="shortAuthors">B. K. Mable, M. A. Alexandrou and M. I. Taylor</title><title type="short">Polyploidy in amphibians and fish</title></titleGroup><creators><creator creatorRole="author" xml:id="cr1" affiliationRef="#a1"><personName><givenNames>B. K.</givenNames><familyName>Mable</familyName></personName></creator><creator creatorRole="author" xml:id="cr2" affiliationRef="#a2"><personName><givenNames>M. A.</givenNames><familyName>Alexandrou</familyName></personName></creator><creator creatorRole="author" xml:id="cr3" affiliationRef="#a2"><personName><givenNames>M. I.</givenNames><familyName>Taylor</familyName></personName></creator></creators><affiliationGroup><affiliation xml:id="a1" countryCode="GB"><unparsedAffiliation>Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK</unparsedAffiliation></affiliation><affiliation xml:id="a2" countryCode="GB"><unparsedAffiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</unparsedAffiliation></affiliation></affiliationGroup><keywordGroup xml:lang="en"><keyword xml:id="k1">polyploidy</keyword><keyword xml:id="k2">amphibians</keyword><keyword xml:id="k3">fish</keyword><keyword xml:id="k4">climate change</keyword><keyword xml:id="k5">unreduced gamete formation</keyword><keyword xml:id="k6">phylogeny</keyword><keyword xml:id="k7">cytogenetics</keyword><keyword xml:id="k8">genome size</keyword></keywordGroup><supportingInformation><p><b>Appendix S1.</b> Glossary of Terms.</p><p><b>Figure S1.</b> Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (<i>Ambystoma Jeffersonian</i> complex of salamanders) and the first polyploid anuran species (<i>Odontophrynus americanus</i>) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak.</p><p><b>Figure S2a.</b> Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed.</p><p><b>Figure S2b.</b> Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic).</p><p><b>Table S1.</b> Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; <link href="http://www.genomesize.com/">http://www.genomesize.com/</link>) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (<link href="http://amphibiaweb.org/">http://amphibiaweb.org/</link>); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, <link href="http://www.iucnredlist.org">http://www.iucnredlist.org</link>). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost <i>et al</i>. 2010; <link href="http://research.amnh.org/vz/herpetology/amphibia/">http://research.amnh.org/vz/herpetology/amphibia/</link>).</p><p><b>Table S2.</b> Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese <i>et al</i>. 2008; <link href="http://www.fishbase.org">http://www.fishbase.org</link>).</p><p>As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.</p><supportingInfoItem><mediaResource alt="supporting info item" href="urn-x:wiley:09528369:media:jzo829:JZO_829_sm_fig-s1"></mediaResource><caption>Supporting info item</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting info item" href="urn-x:wiley:09528369:media:jzo829:JZO_829_sm_fig-s2"></mediaResource><caption>Supporting info item</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting info item" href="urn-x:wiley:09528369:media:jzo829:JZO_829_sm_table-s1"></mediaResource><caption>Supporting info item</caption></supportingInfoItem><supportingInfoItem><mediaResource alt="supporting info item" href="urn-x:wiley:09528369:media:jzo829:JZO_829_sm_table-s2"></mediaResource><caption>Supporting info item</caption></supportingInfoItem></supportingInformation><abstractGroup><abstract type="main" xml:lang="en"><title type="main">Abstract</title><p>Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.</p></abstract></abstractGroup></contentMeta><noteGroup><note xml:id="fn1"><p>Editor: Steven Le Comber</p></note></noteGroup></header></component></istex:document></istex:metadataXml><mods version="3.6"><titleInfo lang="en"><title>Genome duplication in amphibians and fish: an extended synthesis</title></titleInfo><titleInfo type="abbreviated" lang="en"><title>Polyploidy in amphibians and fish</title></titleInfo><titleInfo type="alternative" contentType="CDATA" lang="en"><title>Genome duplication in amphibians and fish: an extended synthesis</title></titleInfo><name type="personal"><namePart type="given">B. K.</namePart><namePart type="family">Mable</namePart><affiliation>Institute of Biodiversity, Animal Health & Comparative Medicine, College of Medical, Veterinary & Life Sciences, University of Glasgow, Glasgow, UK</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">M. A.</namePart><namePart type="family">Alexandrou</namePart><affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</affiliation><role><roleTerm type="text">author</roleTerm></role></name><name type="personal"><namePart type="given">M. I.</namePart><namePart type="family">Taylor</namePart><affiliation>Environment Centre Wales, Molecular Ecology and Fisheries Genetics Laboratory, School of Biological Sciences, College of Natural Sciences, Bangor University, Bangor, UK</affiliation><role><roleTerm type="text">author</roleTerm></role></name><typeOfResource>text</typeOfResource><genre type="review-article" displayLabel="reviewArticle"></genre><originInfo><publisher>Blackwell Publishing Ltd</publisher><place><placeTerm type="text">Oxford, UK</placeTerm></place><dateIssued encoding="w3cdtf">2011-07</dateIssued><edition>Received 10 September 2010; revised 23 February 2011; accepted 25 April 2011</edition><copyrightDate encoding="w3cdtf">2011</copyrightDate></originInfo><language><languageTerm type="code" authority="rfc3066">en</languageTerm><languageTerm type="code" authority="iso639-2b">eng</languageTerm></language><physicalDescription><internetMediaType>text/html</internetMediaType><extent unit="figures">4</extent><extent unit="tables">2</extent><extent unit="references">353</extent><extent unit="words">31420</extent></physicalDescription><abstract lang="en">Whole genome duplication (leading to polyploidy) is widely accepted as an important evolutionary force in plants, but it is less recognized as a driver of animal diversification. Nevertheless, it occurs across a wide range of animals; this review investigates why it is particularly common in fish and amphibians, while rare among other vertebrates. We review the current geographic, ecological and phylogenetic distributions of sexually reproducing polyploid taxa before focusing more specifically on what factors drive polyploid formation and establishment. In summary, (1) polyploidy is phylogenetically restricted in both amphibians and fishes, although entire fish, but not amphibian, lineages are derived from polyploid ancestors. (2) Although mechanisms such as polyspermy are feasible, polyploid formation appears to occur principally through unreduced gamete formation, which can be experimentally induced by temperature or pressure shock in both groups. (3) External reproduction and fertilization in primarily temperate freshwater environments potentially exposes zygotes to temperature stress, which can promote increased production of unreduced gametes. (4) Large numbers of gametes and group breeding in relatively confined areas could increase the probability of compatible gamete combinations in both groups. (5) Both fish and amphibians have a propensity to form reproductively successful hybrids; although the relative frequency of autopolyploidy versus allopolyploidy is difficult to ascertain, multiple origins involving hybridization have been confirmed for a number of species in both groups. (6) Problems with establishment of polyploid lineages associated with minority cytotype exclusion could be overcome in amphibians via assortative mating by acoustic recognition of the same ploidy level, but less attention has been given to chemical or acoustic mechanisms that might operate in fish. (7) There is no strong evidence that polyploid fish or amphibians currently exist in more extreme environments than their diploid progenitors or have broader ecological ranges. (8) Although pathogens could play a role in the relative fitness of polyploid species, particularly given duplication of genes involved in immunity, this remains an understudied field in both fish and amphibians. (9) As in plants, many duplicate copies of genes are retained for long periods of time, indicative of selective maintenance of the duplicate copies, but we find no physiological or other reasons that could explain an advantage for allelic or genetic complexity. (10) Extant polyploid species do not appear to be more or less prone to extinction than related diploids in either group. We conclude that, while polyploid fish and amphibians share a number of attributes facilitating polyploidy, clear drivers of genome duplication do not emerge from the comparison. The lack of a clear association of sexually reproducing polyploids with range expansion, harsh environments, or risk of extinction could suggest that stronger correlations in plants may be driven by shifts in mating system more than ploidy. However, insufficient data currently exist to provide rigorous tests of these hypotheses and we make a plea for zoologists to also consider polyploidy as a possibility in continuing taxonomic surveys.</abstract><subject lang="en"><genre>keywords</genre><topic>polyploidy</topic><topic>amphibians</topic><topic>fish</topic><topic>climate change</topic><topic>unreduced gamete formation</topic><topic>phylogeny</topic><topic>cytogenetics</topic><topic>genome size</topic></subject><relatedItem type="host"><titleInfo><title>Journal of Zoology</title></titleInfo><genre type="journal">journal</genre><note type="content"> Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors. Appendix S1. Glossary of Terms. Figure S1. Distribution of descriptions of new polyploid anuran species by decade. The first naturally occurring polyploid amphibians were described in 1964 (Ambystoma Jeffersonian complex of salamanders) and the first polyploid anuran species (Odontophrynus americanus) was reported in 1966. The peak of new descriptions was in the 1970's, when allozymes and cytogenetics were at their peak. Figure S2a. Distribution of polyploid fish by habitats and breeding site for migratory species. The vast majority of polyploid fish are dependent on freshwater: either living exclusively in freshwater, migrating from marine to freshwater to breed (anadromous) or completing their entire lifecycle within rivers (potamodromous). A small percentage are associated with brackish water and only a very few are catadromous (live in freshwater but migrate to a marine environment to breed. Figure S2b. Distribution of polyploid fish by niche type. Most polyploids either live near the bottom surface (benthopelagic) or in the bottom part of the water column (demersal) rather than on the surface (pelagic). Table S1. Summary of known polyploid anurans (bold face type), along with their closest known diploid relatives, indicating original taxonomy (genus and family) at the time that the polyploids were described, as well as revised taxonomy. References are provided for the first report of polyploidy for each species, as well as those recommending changes to the original taxonomy. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database (Gregory 2005a; http://www.genomesize.com/) but are not available for most of the species listed. Notes on origins of the polyploids were taken from the primary literature. Coordinates for the centre of distributions of polyploid taxa were taken from the maps available through Amphibiaweb (http://amphibiaweb.org/); Krüppen classifications were used to characterize the climates in the relevant regions. Endangered species status and population trends were obtained from the IUCN database (International Union for Conservation of Nature Redlist of Endangered species, http://www.iucnredlist.org). Descriptions of species distributions were obtained from the Amphibian Species of the World database (Frost et al. 2010; http://research.amnh.org/vz/herpetology/amphibia/). Table S2. Summary of known polyploid fish, along with a list of species where polyploidy has been suspected but not confirmed. A description of higher level classifications is provided for comparison with Fig. 2. References are provided for the first report of polyploidy for each species. Chromosome numbers were taken from the original ploidy descriptions; genome sizes were obtained from the Animal Genome Size database. Endangered species status and population trends were obtained from the IUCN Red list database. Notes on distributions, environment, and climate were obtained from Fishbase (Froese et al. 2008; http://www.fishbase.org). As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer‐reviewed and may be re‐organized for online delivery, but are not copy‐edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.Supporting Info Item: Supporting info item - Supporting info item - Supporting info item - Supporting info item - </note><identifier type="ISSN">0952-8369</identifier><identifier type="eISSN">1469-7998</identifier><identifier type="DOI">10.1111/(ISSN)1469-7998</identifier><identifier type="PublisherID">JZO</identifier><part><date>2011</date><detail type="volume"><caption>vol.</caption><number>284</number></detail><detail type="issue"><caption>no.</caption><number>3</number></detail><extent unit="pages"><start>151</start><end>182</end><total>32</total></extent></part></relatedItem><identifier type="istex">54AD7647C7FAB81066FC7E45E4EA0ACE71B0B3A7</identifier><identifier type="DOI">10.1111/j.1469-7998.2011.00829.x</identifier><identifier type="ArticleID">JZO829</identifier><accessCondition type="use and reproduction" contentType="copyright">© 2011 The Authors. 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