The evolutionary dynamics of influenza A virus adaptation to mammalian hosts
Identifieur interne : 001449 ( Main/Merge ); précédent : 001448; suivant : 001450The evolutionary dynamics of influenza A virus adaptation to mammalian hosts
Auteurs : S. Bhatt [Royaume-Uni] ; T. T. Lam [Royaume-Uni] ; S. J. Lycett [Royaume-Uni] ; A. J. Leigh Brown [Royaume-Uni] ; T. A. Bowden [Royaume-Uni] ; E. C. Holmes [États-Unis] ; Y. Guan [République populaire de Chine] ; J. L. N. Wood [Royaume-Uni] ; I. H. Brown [Royaume-Uni] ; P. Kellam [Royaume-Uni] ; O. G. Pybus [Royaume-Uni] ; Ian Brown ; Sharon Brookes ; Anna Germundsson ; Alex Cook ; Susanna Williamson ; Stephen Essen ; Fanny Garcon ; George Gunn ; Manuel Sanchez ; Diogo Marques ; James Wood ; Dan Tucker ; Ian Mccrone ; Julia Gog ; Roberto Saenz ; Meg Staff ; Pablo Murcia ; Wendy Barclay ; Christl Donnelly ; Ruth A. Elderfield ; Paul Kellam ; Greg Baillie ; Eve Coulter ; Barbara Wieland ; Alex Mastin ; John Mccauley ; Andy Leigh Brown ; Sam Lycett ; Mark Woolhouse ; Oliver Pybus ; Samir Bhatt ; Andrew Hayward ; David Ishola ; Alan Archibald ; Tom Freeman ; Bryan Charleston ; Eric Lefevre ; Mick Bailey ; Charlotte Inman ; Chris Stokes ; Kin Chow Chang ; Stephen Dunham ; Gavin White ; Jonathan Nguyen-Van-Tam ; Joanne EnstoneSource :
- Philosophical Transactions of the Royal Society B [ 0962-8436 ] ; 2013.
Abstract
Few questions on infectious disease are more important than understanding how and why avian influenza A viruses successfully emerge in mammalian populations, yet little is known about the rate and nature of the virus’ genetic adaptation in new hosts. Here, we measure, for the first time, the genomic rate of adaptive evolution of swine influenza viruses (SwIV) that originated in birds. By using a curated dataset of more than 24 000 human and swine influenza gene sequences, including 41 newly characterized genomes, we reconstructed the adaptive dynamics of three major SwIV lineages (Eurasian, EA; classical swine, CS; triple reassortant, TR). We found that, following the transfer of the EA lineage from birds to swine in the late 1970s, EA virus genes have undergone substantially faster adaptive evolution than those of the CS lineage, which had circulated among swine for decades. Further, the adaptation rates of the EA lineage antigenic haemagglutinin and neuraminidase genes were unexpectedly high and similar to those observed in human influenza A. We show that the successful establishment of avian influenza viruses in swine is associated with raised adaptive evolution across the entire genome for many years after zoonosis, reflecting the contribution of multiple mutations to the coordinated optimization of viral fitness in a new environment. This dynamics is replicated independently in the polymerase genes of the TR lineage, which established in swine following separate transmission from non-swine hosts.
Url:
DOI: 10.1098/rstb.2012.0382
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<author wicri:is="80%"><name sortKey="Wieland, Barbara" sort="Wieland, Barbara" uniqKey="Wieland B" first="Barbara" last="Wieland">Barbara Wieland</name>
</author>
<author wicri:is="80%"><name sortKey="Mastin, Alex" sort="Mastin, Alex" uniqKey="Mastin A" first="Alex" last="Mastin">Alex Mastin</name>
</author>
<author wicri:is="80%"><name sortKey="Mccauley, John" sort="Mccauley, John" uniqKey="Mccauley J" first="John" last="Mccauley">John Mccauley</name>
</author>
<author wicri:is="80%"><name sortKey="Brown, Andy Leigh" sort="Brown, Andy Leigh" uniqKey="Brown A" first="Andy Leigh" last="Brown">Andy Leigh Brown</name>
</author>
<author wicri:is="80%"><name sortKey="Lycett, Sam" sort="Lycett, Sam" uniqKey="Lycett S" first="Sam" last="Lycett">Sam Lycett</name>
</author>
<author wicri:is="80%"><name sortKey="Woolhouse, Mark" sort="Woolhouse, Mark" uniqKey="Woolhouse M" first="Mark" last="Woolhouse">Mark Woolhouse</name>
</author>
<author wicri:is="80%"><name sortKey="Pybus, Oliver" sort="Pybus, Oliver" uniqKey="Pybus O" first="Oliver" last="Pybus">Oliver Pybus</name>
</author>
<author wicri:is="80%"><name sortKey="Bhatt, Samir" sort="Bhatt, Samir" uniqKey="Bhatt S" first="Samir" last="Bhatt">Samir Bhatt</name>
</author>
<author wicri:is="80%"><name sortKey="Hayward, Andrew" sort="Hayward, Andrew" uniqKey="Hayward A" first="Andrew" last="Hayward">Andrew Hayward</name>
</author>
<author wicri:is="80%"><name sortKey="Ishola, David" sort="Ishola, David" uniqKey="Ishola D" first="David" last="Ishola">David Ishola</name>
</author>
<author wicri:is="80%"><name sortKey="Archibald, Alan" sort="Archibald, Alan" uniqKey="Archibald A" first="Alan" last="Archibald">Alan Archibald</name>
</author>
<author wicri:is="80%"><name sortKey="Freeman, Tom" sort="Freeman, Tom" uniqKey="Freeman T" first="Tom" last="Freeman">Tom Freeman</name>
</author>
<author wicri:is="80%"><name sortKey="Charleston, Bryan" sort="Charleston, Bryan" uniqKey="Charleston B" first="Bryan" last="Charleston">Bryan Charleston</name>
</author>
<author wicri:is="80%"><name sortKey="Lefevre, Eric" sort="Lefevre, Eric" uniqKey="Lefevre E" first="Eric" last="Lefevre">Eric Lefevre</name>
</author>
<author wicri:is="80%"><name sortKey="Bailey, Mick" sort="Bailey, Mick" uniqKey="Bailey M" first="Mick" last="Bailey">Mick Bailey</name>
</author>
<author wicri:is="80%"><name sortKey="Inman, Charlotte" sort="Inman, Charlotte" uniqKey="Inman C" first="Charlotte" last="Inman">Charlotte Inman</name>
</author>
<author wicri:is="80%"><name sortKey="Stokes, Chris" sort="Stokes, Chris" uniqKey="Stokes C" first="Chris" last="Stokes">Chris Stokes</name>
</author>
<author wicri:is="80%"><name sortKey="Chang, Kin Chow" sort="Chang, Kin Chow" uniqKey="Chang K" first="Kin Chow" last="Chang">Kin Chow Chang</name>
</author>
<author wicri:is="80%"><name sortKey="Dunham, Stephen" sort="Dunham, Stephen" uniqKey="Dunham S" first="Stephen" last="Dunham">Stephen Dunham</name>
</author>
<author wicri:is="80%"><name sortKey="White, Gavin" sort="White, Gavin" uniqKey="White G" first="Gavin" last="White">Gavin White</name>
</author>
<author wicri:is="80%"><name sortKey="Nguyen Van Tam, Jonathan" sort="Nguyen Van Tam, Jonathan" uniqKey="Nguyen Van Tam J" first="Jonathan" last="Nguyen-Van-Tam">Jonathan Nguyen-Van-Tam</name>
</author>
<author wicri:is="80%"><name sortKey="Enstone, Joanne" sort="Enstone, Joanne" uniqKey="Enstone J" first="Joanne" last="Enstone">Joanne Enstone</name>
</author>
</analytic>
<monogr></monogr>
<series><title level="j" type="main">Philosophical Transactions of the Royal Society B</title>
<title level="j" type="issue">Discussion Meeting Issue 'Next-generation molecular and evolutionary epidemiology of infectious disease' compiled and edited by O. G. Pybus, C. Fraser and A. Rambaut</title>
<title level="j" type="abbrev">Phil. Trans. R. Soc. B</title>
<idno type="ISSN">0962-8436</idno>
<idno type="eISSN">1471-2970</idno>
<imprint><publisher>The Royal Society</publisher>
<date type="published">2013</date>
<biblScope unit="vol">368</biblScope>
<biblScope unit="issue">1614</biblScope>
</imprint>
<idno type="ISSN">0962-8436</idno>
</series>
</biblStruct>
</sourceDesc>
<seriesStmt><idno type="ISSN">0962-8436</idno>
</seriesStmt>
</fileDesc>
<profileDesc><textClass></textClass>
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<front><div type="abstract">Few questions on infectious disease are more important than understanding how and why avian influenza A viruses successfully emerge in mammalian populations, yet little is known about the rate and nature of the virus’ genetic adaptation in new hosts. Here, we measure, for the first time, the genomic rate of adaptive evolution of swine influenza viruses (SwIV) that originated in birds. By using a curated dataset of more than 24 000 human and swine influenza gene sequences, including 41 newly characterized genomes, we reconstructed the adaptive dynamics of three major SwIV lineages (Eurasian, EA; classical swine, CS; triple reassortant, TR). We found that, following the transfer of the EA lineage from birds to swine in the late 1970s, EA virus genes have undergone substantially faster adaptive evolution than those of the CS lineage, which had circulated among swine for decades. Further, the adaptation rates of the EA lineage antigenic haemagglutinin and neuraminidase genes were unexpectedly high and similar to those observed in human influenza A. We show that the successful establishment of avian influenza viruses in swine is associated with raised adaptive evolution across the entire genome for many years after zoonosis, reflecting the contribution of multiple mutations to the coordinated optimization of viral fitness in a new environment. This dynamics is replicated independently in the polymerase genes of the TR lineage, which established in swine following separate transmission from non-swine hosts.</div>
</front>
</TEI>
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