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Large-Scale Phylogenomic Analysis Reveals the Complex Evolutionary History of Rabies Virus in Multiple Carnivore Hosts.

Identifieur interne : 001B49 ( PubMed/Checkpoint ); précédent : 001B48; suivant : 001B50

Large-Scale Phylogenomic Analysis Reveals the Complex Evolutionary History of Rabies Virus in Multiple Carnivore Hosts.

Auteurs : Cécile Troupin [France] ; Laurent Dacheux [France] ; Marion Tanguy [France] ; Claude Sabeta [Afrique du Sud] ; Hervé Blanc [France] ; Christiane Bouchier [France] ; Marco Vignuzzi [France] ; Sebastián Duchene [Australie] ; Edward C. Holmes [Australie] ; Hervé Bourhy [France]

Source :

RBID : pubmed:27977811

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English descriptors

Abstract

The natural evolution of rabies virus (RABV) provides a potent example of multiple host shifts and an important opportunity to determine the mechanisms that underpin viral emergence. Using 321 genome sequences spanning an unprecedented diversity of RABV, we compared evolutionary rates and selection pressures in viruses sampled from multiple primary host shifts that occurred on various continents. Two major phylogenetic groups, bat-related RABV and dog-related RABV, experiencing markedly different evolutionary dynamics were identified. While no correlation between time and genetic divergence was found in bat-related RABV, the evolution of dog-related RABV followed a generally clock-like structure, although with a relatively low evolutionary rate. Subsequent molecular clock dating indicated that dog-related RABV likely underwent a rapid global spread following the intensification of intercontinental trade starting in the 15th century. Strikingly, although dog RABV has jumped to various wildlife species from the order Carnivora, we found no clear evidence that these host-jumping events involved adaptive evolution, with RABV instead characterized by strong purifying selection, suggesting that ecological processes also play an important role in shaping patterns of emergence. However, specific amino acid changes were associated with the parallel emergence of RABV in ferret-badgers in Asia, and some host shifts were associated with increases in evolutionary rate, particularly in the ferret-badger and mongoose, implying that changes in host species can have important impacts on evolutionary dynamics.

DOI: 10.1371/journal.ppat.1006041
PubMed: 27977811


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Le document en format XML

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<term>Genome, Viral</term>
<term>High-Throughput Nucleotide Sequencing</term>
<term>Host-Pathogen Interactions (physiology)</term>
<term>Humans</term>
<term>Phylogeny</term>
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<term>ARN viral</term>
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<term>Rabies</term>
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<div type="abstract" xml:lang="en">The natural evolution of rabies virus (RABV) provides a potent example of multiple host shifts and an important opportunity to determine the mechanisms that underpin viral emergence. Using 321 genome sequences spanning an unprecedented diversity of RABV, we compared evolutionary rates and selection pressures in viruses sampled from multiple primary host shifts that occurred on various continents. Two major phylogenetic groups, bat-related RABV and dog-related RABV, experiencing markedly different evolutionary dynamics were identified. While no correlation between time and genetic divergence was found in bat-related RABV, the evolution of dog-related RABV followed a generally clock-like structure, although with a relatively low evolutionary rate. Subsequent molecular clock dating indicated that dog-related RABV likely underwent a rapid global spread following the intensification of intercontinental trade starting in the 15th century. Strikingly, although dog RABV has jumped to various wildlife species from the order Carnivora, we found no clear evidence that these host-jumping events involved adaptive evolution, with RABV instead characterized by strong purifying selection, suggesting that ecological processes also play an important role in shaping patterns of emergence. However, specific amino acid changes were associated with the parallel emergence of RABV in ferret-badgers in Asia, and some host shifts were associated with increases in evolutionary rate, particularly in the ferret-badger and mongoose, implying that changes in host species can have important impacts on evolutionary dynamics.</div>
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<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1006041</ELocationID>
<Abstract>
<AbstractText>The natural evolution of rabies virus (RABV) provides a potent example of multiple host shifts and an important opportunity to determine the mechanisms that underpin viral emergence. Using 321 genome sequences spanning an unprecedented diversity of RABV, we compared evolutionary rates and selection pressures in viruses sampled from multiple primary host shifts that occurred on various continents. Two major phylogenetic groups, bat-related RABV and dog-related RABV, experiencing markedly different evolutionary dynamics were identified. While no correlation between time and genetic divergence was found in bat-related RABV, the evolution of dog-related RABV followed a generally clock-like structure, although with a relatively low evolutionary rate. Subsequent molecular clock dating indicated that dog-related RABV likely underwent a rapid global spread following the intensification of intercontinental trade starting in the 15th century. Strikingly, although dog RABV has jumped to various wildlife species from the order Carnivora, we found no clear evidence that these host-jumping events involved adaptive evolution, with RABV instead characterized by strong purifying selection, suggesting that ecological processes also play an important role in shaping patterns of emergence. However, specific amino acid changes were associated with the parallel emergence of RABV in ferret-badgers in Asia, and some host shifts were associated with increases in evolutionary rate, particularly in the ferret-badger and mongoose, implying that changes in host species can have important impacts on evolutionary dynamics.</AbstractText>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Troupin</LastName>
<ForeName>Cécile</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unit Lyssavirus Dynamics and Host Adaptation, WHO Collaborating Centre for Reference and Research on Rabies, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dacheux</LastName>
<ForeName>Laurent</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unit Lyssavirus Dynamics and Host Adaptation, WHO Collaborating Centre for Reference and Research on Rabies, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tanguy</LastName>
<ForeName>Marion</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unit Lyssavirus Dynamics and Host Adaptation, WHO Collaborating Centre for Reference and Research on Rabies, Paris, France.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Genomics Platform, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sabeta</LastName>
<ForeName>Claude</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Agricultural Research Council, Onderstepoort Veterinary Institute, OIE Rabies Reference Laboratory, Pretoria, South Africa.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Blanc</LastName>
<ForeName>Hervé</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Centre National de la Recherche Scientifique UMR 3569, Viral Populations and Pathogenesis Unit, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bouchier</LastName>
<ForeName>Christiane</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Genomics Platform, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Vignuzzi</LastName>
<ForeName>Marco</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Centre National de la Recherche Scientifique UMR 3569, Viral Populations and Pathogenesis Unit, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Duchene</LastName>
<ForeName>Sebastián</ForeName>
<Initials>S</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0002-2863-0907</Identifier>
<AffiliationInfo>
<Affiliation>Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Centre for Systems Genomics, University of Melbourne, Parkville, Victoria, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Holmes</LastName>
<ForeName>Edward C</ForeName>
<Initials>EC</Initials>
<AffiliationInfo>
<Affiliation>Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Bourhy</LastName>
<ForeName>Hervé</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Institut Pasteur, Unit Lyssavirus Dynamics and Host Adaptation, WHO Collaborating Centre for Reference and Research on Rabies, Paris, France.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2016</Year>
<Month>12</Month>
<Day>15</Day>
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<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D000835" MajorTopicYN="N">Animals, Wild</DescriptorName>
<QualifierName UI="Q000821" MajorTopicYN="Y">virology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005075" MajorTopicYN="Y">Biological Evolution</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002335" MajorTopicYN="N">Carnivora</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016679" MajorTopicYN="N">Genome, Viral</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D059014" MajorTopicYN="N">High-Throughput Nucleotide Sequencing</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D054884" MajorTopicYN="N">Host-Pathogen Interactions</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010802" MajorTopicYN="N">Phylogeny</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D012367" MajorTopicYN="N">RNA, Viral</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011818" MajorTopicYN="N">Rabies</DescriptorName>
<QualifierName UI="Q000662" MajorTopicYN="Y">veterinary</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D011820" MajorTopicYN="N">Rabies virus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D020133" MajorTopicYN="N">Reverse Transcriptase Polymerase Chain Reaction</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015047" MajorTopicYN="N">Zoonoses</DescriptorName>
<QualifierName UI="Q000635" MajorTopicYN="N">transmission</QualifierName>
</MeshHeading>
</MeshHeadingList>
<CoiStatement>The authors have declared that no competing interests exist.</CoiStatement>
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<li>Afrique du Sud</li>
<li>Australie</li>
<li>France</li>
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<li>Nouvelle-Galles du Sud</li>
<li>Île-de-France</li>
</region>
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<li>Paris</li>
<li>Sydney</li>
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<li>Université de Sydney</li>
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<name sortKey="Troupin, Cecile" sort="Troupin, Cecile" uniqKey="Troupin C" first="Cécile" last="Troupin">Cécile Troupin</name>
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<name sortKey="Blanc, Herve" sort="Blanc, Herve" uniqKey="Blanc H" first="Hervé" last="Blanc">Hervé Blanc</name>
<name sortKey="Bouchier, Christiane" sort="Bouchier, Christiane" uniqKey="Bouchier C" first="Christiane" last="Bouchier">Christiane Bouchier</name>
<name sortKey="Bourhy, Herve" sort="Bourhy, Herve" uniqKey="Bourhy H" first="Hervé" last="Bourhy">Hervé Bourhy</name>
<name sortKey="Dacheux, Laurent" sort="Dacheux, Laurent" uniqKey="Dacheux L" first="Laurent" last="Dacheux">Laurent Dacheux</name>
<name sortKey="Tanguy, Marion" sort="Tanguy, Marion" uniqKey="Tanguy M" first="Marion" last="Tanguy">Marion Tanguy</name>
<name sortKey="Vignuzzi, Marco" sort="Vignuzzi, Marco" uniqKey="Vignuzzi M" first="Marco" last="Vignuzzi">Marco Vignuzzi</name>
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<country name="Afrique du Sud">
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<name sortKey="Sabeta, Claude" sort="Sabeta, Claude" uniqKey="Sabeta C" first="Claude" last="Sabeta">Claude Sabeta</name>
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<country name="Australie">
<region name="Nouvelle-Galles du Sud">
<name sortKey="Duchene, Sebastian" sort="Duchene, Sebastian" uniqKey="Duchene S" first="Sebastián" last="Duchene">Sebastián Duchene</name>
</region>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C" last="Holmes">Edward C. Holmes</name>
</country>
</tree>
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</record>

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