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Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

Identifieur interne : 001051 ( Main/Exploration ); précédent : 001050; suivant : 001052

Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.

Auteurs : Tao Ma [République populaire de Chine] ; Kun Wang [République populaire de Chine] ; Quanjun Hu [République populaire de Chine] ; Zhenxiang Xi [République populaire de Chine] ; Dongshi Wan [République populaire de Chine] ; Qian Wang [République populaire de Chine] ; Jianju Feng [République populaire de Chine] ; Dechun Jiang [République populaire de Chine] ; Hamid Ahani [Iran] ; Richard J. Abbott [Royaume-Uni] ; Martin Lascoux [Suède] ; Eviatar Nevo [République populaire de Chine] ; Jianquan Liu [République populaire de Chine]

Source :

RBID : pubmed:29279400

Descripteurs français

English descriptors

Abstract

How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species, Populus euphratica and Populus pruinosa, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.

DOI: 10.1073/pnas.1713288114
PubMed: 29279400
PubMed Central: PMC5777044


Affiliations:


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Le document en format XML

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<term>Biological Evolution (MeSH)</term>
<term>Chromosome Mapping (MeSH)</term>
<term>Chromosomes, Plant (genetics)</term>
<term>Genetic Speciation (MeSH)</term>
<term>Genome, Plant (MeSH)</term>
<term>Genomic Islands (MeSH)</term>
<term>Polymorphism, Genetic (MeSH)</term>
<term>Populus (genetics)</term>
</keywords>
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<term>Cartographie chromosomique (MeSH)</term>
<term>Chromosomes de plante (génétique)</term>
<term>Génome végétal (MeSH)</term>
<term>Ilots génomiques (MeSH)</term>
<term>Polymorphisme génétique (MeSH)</term>
<term>Populus (génétique)</term>
<term>Spéciation génétique (MeSH)</term>
<term>Évolution biologique (MeSH)</term>
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<term>Chromosomes, Plant</term>
<term>Populus</term>
</keywords>
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<term>Chromosomes de plante</term>
<term>Populus</term>
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<term>Biological Evolution</term>
<term>Chromosome Mapping</term>
<term>Genetic Speciation</term>
<term>Genome, Plant</term>
<term>Genomic Islands</term>
<term>Polymorphism, Genetic</term>
</keywords>
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<term>Cartographie chromosomique</term>
<term>Génome végétal</term>
<term>Ilots génomiques</term>
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<div type="abstract" xml:lang="en">How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species,
<i>Populus euphratica</i>
and
<i>Populus pruinosa</i>
, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.</div>
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<ArticleTitle>Ancient polymorphisms and divergence hitchhiking contribute to genomic islands of divergence within a poplar species complex.</ArticleTitle>
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<MedlinePgn>E236-E243</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1073/pnas.1713288114</ELocationID>
<Abstract>
<AbstractText>How genome divergence eventually leads to speciation is a topic of prime evolutionary interest. Genomic islands of elevated divergence are frequently reported between diverging lineages, and their size is expected to increase with time and gene flow under the speciation-with-gene-flow model. However, such islands can also result from divergent sorting of ancient polymorphisms, recent ecological selection regardless of gene flow, and/or recurrent background selection and selective sweeps in low-recombination regions. It is challenging to disentangle these nonexclusive alternatives, but here we attempt to do this in an analysis of what drove genomic divergence between four lineages comprising a species complex of desert poplar trees. Within this complex we found that two morphologically delimited species,
<i>Populus euphratica</i>
and
<i>Populus pruinosa</i>
, were paraphyletic while the four lineages exhibited contrasting levels of gene flow and divergence times, providing a good system for testing hypotheses on the origin of divergence islands. We show that the size and number of genomic islands that distinguish lineages are not associated with either rate of recent gene flow or time of divergence. Instead, they are most likely derived from divergent sorting of ancient polymorphisms and divergence hitchhiking. We found that highly diverged genes under lineage-specific selection and putatively involved in ecological and morphological divergence occur both within and outside these islands. Our results highlight the need to incorporate demography, absolute divergence measurement, and gene flow rate to explain the formation of genomic islands and to identify potential genomic regions involved in speciation.</AbstractText>
<CopyrightInformation>Copyright © 2018 the Author(s). Published by PNAS.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Ma</LastName>
<ForeName>Tao</ForeName>
<Initials>T</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Kun</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hu</LastName>
<ForeName>Quanjun</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Xi</LastName>
<ForeName>Zhenxiang</ForeName>
<Initials>Z</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wan</LastName>
<ForeName>Dongshi</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Wang</LastName>
<ForeName>Qian</ForeName>
<Initials>Q</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Feng</LastName>
<ForeName>Jianju</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Jiang</LastName>
<ForeName>Dechun</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>State Key Laboratory of Grassland Agro-ecosystem, College of Life Sciences, Lanzhou University, Lanzhou 730000, People's Republic of China.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Ahani</LastName>
<ForeName>Hamid</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Natural Resources and Watershed Management Administration of Khorasan Razavi, Khorasan 9177948974, Iran.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Abbott</LastName>
<ForeName>Richard J</ForeName>
<Initials>RJ</Initials>
<AffiliationInfo>
<Affiliation>School of Biology, University of St. Andrews, St. Andrews, Fife KY16 9TH, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Lascoux</LastName>
<ForeName>Martin</ForeName>
<Initials>M</Initials>
<Identifier Source="ORCID">0000-0003-1699-9042</Identifier>
<AffiliationInfo>
<Affiliation>Department of Ecology and Genetics, Evolutionary Biology Center and Science for Life Laboratory, Uppsala University, Uppsala 75236, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Nevo</LastName>
<ForeName>Eviatar</ForeName>
<Initials>E</Initials>
<AffiliationInfo>
<Affiliation>Institute of Evolution, University of Haifa, Mount Carmel, Haifa 3498838, Israel liujq@nwipb.cas.cn nevo@research.haifa.ac.il.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Liu</LastName>
<ForeName>Jianquan</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Key Laboratory of Bio-Resource and Eco-Environment of Ministry of Education, College of Life Sciences, Sichuan University, Chengdu 610065, People's Republic of China; liujq@nwipb.cas.cn nevo@research.haifa.ac.il.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>12</Month>
<Day>26</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Proc Natl Acad Sci U S A</MedlineTA>
<NlmUniqueID>7505876</NlmUniqueID>
<ISSNLinking>0027-8424</ISSNLinking>
</MedlineJournalInfo>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D005075" MajorTopicYN="Y">Biological Evolution</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002874" MajorTopicYN="N">Chromosome Mapping</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032461" MajorTopicYN="N">Chromosomes, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D049810" MajorTopicYN="Y">Genetic Speciation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018745" MajorTopicYN="N">Genome, Plant</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D044404" MajorTopicYN="Y">Genomic Islands</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011110" MajorTopicYN="Y">Polymorphism, Genetic</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">gene flow</Keyword>
<Keyword MajorTopicYN="Y">genome divergence</Keyword>
<Keyword MajorTopicYN="Y">natural selection</Keyword>
<Keyword MajorTopicYN="Y">paraphyletic</Keyword>
<Keyword MajorTopicYN="Y">speciation</Keyword>
</KeywordList>
<CoiStatement>The authors declare no conflict of interest.</CoiStatement>
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