The evolutionary dynamics of influenza A virus adaptation to mammalian hosts
Identifieur interne : 001428 ( Main/Exploration ); précédent : 001427; suivant : 001429The 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
Affiliations:
- Royaume-Uni, République populaire de Chine, États-Unis
- Angleterre, Angleterre de l'Est, Maryland, Oxfordshire, Pennsylvanie, Écosse
- Cambridge, Oxford, University Park (Pennsylvanie), Édimbourg
- Université d'Oxford, Université d'Édimbourg, Université d'État de Pennsylvanie, Université de Cambridge
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J." last="Leigh Brown">A. J. Leigh Brown</name><affiliation wicri:level="4"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Institute of Evolutionary Biology, University of Edinburgh, Edinburgh</wicri:regionArea><placeName><settlement type="city">Édimbourg</settlement><region type="country">Écosse</region></placeName><orgName type="university">Université d'Édimbourg</orgName></affiliation></author><author><name sortKey="Bowden, T A" sort="Bowden, T A" uniqKey="Bowden T" first="T. A." last="Bowden">T. A. Bowden</name><affiliation wicri:level="4"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Division of Structural Biology, Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford</wicri:regionArea><placeName><settlement type="city">Oxford</settlement><region type="country">Angleterre</region><region type="comté" nuts="2">Oxfordshire</region></placeName><orgName type="university">Université d'Oxford</orgName></affiliation></author><author><name sortKey="Holmes, E C" sort="Holmes, E C" uniqKey="Holmes E" first="E. C." last="Holmes">E. C. Holmes</name><affiliation wicri:level="4"><country xml:lang="fr">États-Unis</country><wicri:regionArea>Mueller Laboratory, Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA</wicri:regionArea><placeName><region type="state">Pennsylvanie</region><settlement type="city">University Park (Pennsylvanie)</settlement></placeName><orgName type="university">Université d'État de Pennsylvanie</orgName></affiliation><affiliation wicri:level="2"><country xml:lang="fr">États-Unis</country><wicri:regionArea>Fogarty International Center, National Institutes of Health, Bethesda, MD</wicri:regionArea><placeName><region type="state">Maryland</region></placeName></affiliation></author><author><name sortKey="Guan, Y" sort="Guan, Y" uniqKey="Guan Y" first="Y." last="Guan">Y. Guan</name><affiliation wicri:level="1"><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>Li Ka Shing Faculty of Medicine, University of Hong Kong, Hong Kong</wicri:regionArea><wicri:noRegion>Hong Kong</wicri:noRegion></affiliation></author><author><name sortKey="Wood, J L N" sort="Wood, J L N" uniqKey="Wood J" first="J. L. N." last="Wood">J. L. N. Wood</name><affiliation wicri:level="4"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Cambridge Infectious Diseases Consortium, University of Cambridge, Cambridge</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Brown, I H" sort="Brown, I H" uniqKey="Brown I" first="I. H." last="Brown">I. H. Brown</name><affiliation wicri:level="1"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Animal Health and Veterinary Laboratories Agency, Weybridge</wicri:regionArea><wicri:noRegion>Weybridge</wicri:noRegion></affiliation></author><author><name sortKey="Kellam, P" sort="Kellam, P" uniqKey="Kellam P" first="P." last="Kellam">P. Kellam</name><affiliation wicri:level="1"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Wellcome Trust Sanger Institute, Hinxton</wicri:regionArea><wicri:noRegion>Hinxton</wicri:noRegion></affiliation></author><author><name sortKey="Pybus, O G" sort="Pybus, O G" uniqKey="Pybus O" first="O. G." last="Pybus">O. G. Pybus</name><affiliation wicri:level="4"><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Zoology, University of Oxford, Oxford</wicri:regionArea><placeName><settlement type="city">Oxford</settlement><region type="country">Angleterre</region><region type="comté" nuts="2">Oxfordshire</region></placeName><orgName type="university">Université d'Oxford</orgName></affiliation><affiliation wicri:level="1"><country wicri:rule="url">Royaume-Uni</country></affiliation></author><author wicri:is="80%"><name sortKey="Brown, Ian" sort="Brown, Ian" uniqKey="Brown I" first="Ian" last="Brown">Ian Brown</name></author><author wicri:is="80%"><name sortKey="Brookes, Sharon" sort="Brookes, Sharon" uniqKey="Brookes S" first="Sharon" last="Brookes">Sharon Brookes</name></author><author wicri:is="80%"><name sortKey="Germundsson, Anna" sort="Germundsson, Anna" uniqKey="Germundsson A" first="Anna" last="Germundsson">Anna Germundsson</name></author><author wicri:is="80%"><name sortKey="Cook, Alex" sort="Cook, Alex" uniqKey="Cook A" first="Alex" last="Cook">Alex Cook</name></author><author wicri:is="80%"><name sortKey="Williamson, Susanna" sort="Williamson, Susanna" uniqKey="Williamson S" first="Susanna" last="Williamson">Susanna Williamson</name></author><author wicri:is="80%"><name sortKey="Essen, Stephen" sort="Essen, Stephen" uniqKey="Essen S" first="Stephen" last="Essen">Stephen Essen</name></author><author wicri:is="80%"><name sortKey="Garcon, Fanny" sort="Garcon, Fanny" uniqKey="Garcon F" first="Fanny" last="Garcon">Fanny Garcon</name></author><author wicri:is="80%"><name sortKey="Gunn, George" sort="Gunn, George" uniqKey="Gunn G" first="George" last="Gunn">George Gunn</name></author><author wicri:is="80%"><name sortKey="Sanchez, Manuel" sort="Sanchez, Manuel" uniqKey="Sanchez M" first="Manuel" last="Sanchez">Manuel Sanchez</name></author><author wicri:is="80%"><name sortKey="Marques, Diogo" sort="Marques, Diogo" uniqKey="Marques D" first="Diogo" last="Marques">Diogo Marques</name></author><author wicri:is="80%"><name sortKey="Wood, James" sort="Wood, James" uniqKey="Wood J" first="James" last="Wood">James Wood</name></author><author wicri:is="80%"><name sortKey="Tucker, Dan" sort="Tucker, Dan" uniqKey="Tucker D" first="Dan" last="Tucker">Dan Tucker</name></author><author wicri:is="80%"><name sortKey="Mccrone, Ian" sort="Mccrone, Ian" uniqKey="Mccrone I" first="Ian" last="Mccrone">Ian Mccrone</name></author><author wicri:is="80%"><name sortKey="Gog, Julia" sort="Gog, Julia" uniqKey="Gog J" first="Julia" last="Gog">Julia Gog</name></author><author wicri:is="80%"><name sortKey="Saenz, Roberto" sort="Saenz, Roberto" uniqKey="Saenz R" first="Roberto" last="Saenz">Roberto Saenz</name></author><author wicri:is="80%"><name sortKey="Staff, Meg" sort="Staff, Meg" uniqKey="Staff M" first="Meg" last="Staff">Meg Staff</name></author><author wicri:is="80%"><name sortKey="Murcia, Pablo" sort="Murcia, Pablo" uniqKey="Murcia P" first="Pablo" last="Murcia">Pablo Murcia</name></author><author wicri:is="80%"><name sortKey="Barclay, Wendy" sort="Barclay, Wendy" uniqKey="Barclay W" first="Wendy" last="Barclay">Wendy Barclay</name></author><author wicri:is="80%"><name sortKey="Donnelly, Christl" sort="Donnelly, Christl" uniqKey="Donnelly C" first="Christl" last="Donnelly">Christl Donnelly</name></author><author wicri:is="80%"><name sortKey="Elderfield, Ruth A" sort="Elderfield, Ruth A" uniqKey="Elderfield R" first="Ruth A." last="Elderfield">Ruth A. Elderfield</name></author><author wicri:is="80%"><name sortKey="Kellam, Paul" sort="Kellam, Paul" uniqKey="Kellam P" first="Paul" last="Kellam">Paul Kellam</name></author><author wicri:is="80%"><name sortKey="Baillie, Greg" sort="Baillie, Greg" uniqKey="Baillie G" first="Greg" last="Baillie">Greg Baillie</name></author><author wicri:is="80%"><name sortKey="Coulter, Eve" sort="Coulter, Eve" uniqKey="Coulter E" first="Eve" last="Coulter">Eve Coulter</name></author><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></profileDesc></teiHeader><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><affiliations><list><country><li>Royaume-Uni</li><li>République populaire de Chine</li><li>États-Unis</li></country><region><li>Angleterre</li><li>Angleterre de l'Est</li><li>Maryland</li><li>Oxfordshire</li><li>Pennsylvanie</li><li>Écosse</li></region><settlement><li>Cambridge</li><li>Oxford</li><li>University Park (Pennsylvanie)</li><li>Édimbourg</li></settlement><orgName><li>Université d'Oxford</li><li>Université d'Édimbourg</li><li>Université d'État de Pennsylvanie</li><li>Université de Cambridge</li></orgName></list><tree><noCountry><name sortKey="Archibald, Alan" sort="Archibald, Alan" uniqKey="Archibald A" first="Alan" last="Archibald">Alan Archibald</name><name sortKey="Bailey, Mick" sort="Bailey, Mick" uniqKey="Bailey M" first="Mick" last="Bailey">Mick Bailey</name><name sortKey="Baillie, Greg" sort="Baillie, Greg" uniqKey="Baillie G" first="Greg" last="Baillie">Greg Baillie</name><name sortKey="Barclay, Wendy" sort="Barclay, Wendy" uniqKey="Barclay W" first="Wendy" last="Barclay">Wendy Barclay</name><name sortKey="Bhatt, Samir" sort="Bhatt, Samir" uniqKey="Bhatt S" first="Samir" last="Bhatt">Samir Bhatt</name><name sortKey="Brookes, Sharon" sort="Brookes, Sharon" uniqKey="Brookes S" first="Sharon" last="Brookes">Sharon Brookes</name><name sortKey="Brown, Andy Leigh" sort="Brown, Andy Leigh" uniqKey="Brown A" first="Andy Leigh" last="Brown">Andy Leigh Brown</name><name sortKey="Brown, Ian" sort="Brown, Ian" uniqKey="Brown I" first="Ian" last="Brown">Ian Brown</name><name sortKey="Chang, Kin Chow" sort="Chang, Kin Chow" uniqKey="Chang K" first="Kin Chow" last="Chang">Kin Chow Chang</name><name sortKey="Charleston, Bryan" sort="Charleston, Bryan" uniqKey="Charleston B" first="Bryan" last="Charleston">Bryan Charleston</name><name sortKey="Cook, Alex" sort="Cook, Alex" uniqKey="Cook A" first="Alex" last="Cook">Alex Cook</name><name sortKey="Coulter, Eve" sort="Coulter, Eve" uniqKey="Coulter E" first="Eve" last="Coulter">Eve Coulter</name><name sortKey="Donnelly, Christl" sort="Donnelly, Christl" uniqKey="Donnelly C" first="Christl" last="Donnelly">Christl Donnelly</name><name sortKey="Dunham, Stephen" sort="Dunham, Stephen" uniqKey="Dunham S" first="Stephen" last="Dunham">Stephen Dunham</name><name sortKey="Elderfield, Ruth A" sort="Elderfield, Ruth A" uniqKey="Elderfield R" first="Ruth A." last="Elderfield">Ruth A. Elderfield</name><name sortKey="Enstone, Joanne" sort="Enstone, Joanne" uniqKey="Enstone J" first="Joanne" last="Enstone">Joanne Enstone</name><name sortKey="Essen, Stephen" sort="Essen, Stephen" uniqKey="Essen S" first="Stephen" last="Essen">Stephen Essen</name><name sortKey="Freeman, Tom" sort="Freeman, Tom" uniqKey="Freeman T" first="Tom" last="Freeman">Tom Freeman</name><name sortKey="Garcon, Fanny" sort="Garcon, Fanny" uniqKey="Garcon F" first="Fanny" last="Garcon">Fanny Garcon</name><name sortKey="Germundsson, Anna" sort="Germundsson, Anna" uniqKey="Germundsson A" first="Anna" last="Germundsson">Anna Germundsson</name><name sortKey="Gog, Julia" sort="Gog, Julia" uniqKey="Gog J" first="Julia" last="Gog">Julia Gog</name><name sortKey="Gunn, George" sort="Gunn, George" uniqKey="Gunn G" first="George" last="Gunn">George Gunn</name><name sortKey="Hayward, Andrew" sort="Hayward, Andrew" uniqKey="Hayward A" first="Andrew" last="Hayward">Andrew Hayward</name><name sortKey="Inman, Charlotte" sort="Inman, Charlotte" uniqKey="Inman C" first="Charlotte" last="Inman">Charlotte Inman</name><name sortKey="Ishola, David" sort="Ishola, David" uniqKey="Ishola D" first="David" last="Ishola">David Ishola</name><name sortKey="Kellam, Paul" sort="Kellam, Paul" uniqKey="Kellam P" first="Paul" last="Kellam">Paul Kellam</name><name sortKey="Lefevre, Eric" sort="Lefevre, Eric" uniqKey="Lefevre E" first="Eric" last="Lefevre">Eric Lefevre</name><name sortKey="Lycett, Sam" sort="Lycett, Sam" uniqKey="Lycett S" first="Sam" last="Lycett">Sam Lycett</name><name sortKey="Marques, Diogo" sort="Marques, Diogo" uniqKey="Marques D" first="Diogo" last="Marques">Diogo Marques</name><name sortKey="Mastin, Alex" sort="Mastin, Alex" uniqKey="Mastin A" first="Alex" last="Mastin">Alex Mastin</name><name sortKey="Mccauley, John" sort="Mccauley, John" uniqKey="Mccauley J" first="John" last="Mccauley">John Mccauley</name><name sortKey="Mccrone, Ian" sort="Mccrone, Ian" uniqKey="Mccrone I" first="Ian" last="Mccrone">Ian Mccrone</name><name sortKey="Murcia, Pablo" sort="Murcia, Pablo" uniqKey="Murcia P" first="Pablo" last="Murcia">Pablo Murcia</name><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><name sortKey="Pybus, Oliver" sort="Pybus, Oliver" uniqKey="Pybus O" first="Oliver" last="Pybus">Oliver Pybus</name><name sortKey="Saenz, Roberto" sort="Saenz, Roberto" uniqKey="Saenz R" first="Roberto" last="Saenz">Roberto Saenz</name><name sortKey="Sanchez, Manuel" sort="Sanchez, Manuel" uniqKey="Sanchez M" first="Manuel" last="Sanchez">Manuel Sanchez</name><name sortKey="Staff, Meg" sort="Staff, Meg" uniqKey="Staff M" first="Meg" last="Staff">Meg Staff</name><name sortKey="Stokes, Chris" sort="Stokes, Chris" uniqKey="Stokes C" first="Chris" last="Stokes">Chris Stokes</name><name sortKey="Tucker, Dan" sort="Tucker, Dan" uniqKey="Tucker D" first="Dan" last="Tucker">Dan Tucker</name><name sortKey="White, Gavin" sort="White, Gavin" uniqKey="White G" first="Gavin" last="White">Gavin White</name><name sortKey="Wieland, Barbara" sort="Wieland, Barbara" uniqKey="Wieland B" first="Barbara" last="Wieland">Barbara Wieland</name><name sortKey="Williamson, Susanna" sort="Williamson, Susanna" uniqKey="Williamson S" first="Susanna" last="Williamson">Susanna Williamson</name><name sortKey="Wood, James" sort="Wood, James" uniqKey="Wood J" first="James" last="Wood">James Wood</name><name sortKey="Woolhouse, Mark" sort="Woolhouse, Mark" uniqKey="Woolhouse M" first="Mark" last="Woolhouse">Mark Woolhouse</name></noCountry><country name="Royaume-Uni"><region name="Angleterre"><name sortKey="Bhatt, S" sort="Bhatt, S" uniqKey="Bhatt S" first="S." last="Bhatt">S. Bhatt</name></region><name sortKey="Bhatt, S" sort="Bhatt, S" uniqKey="Bhatt S" first="S." last="Bhatt">S. Bhatt</name><name sortKey="Bowden, T A" sort="Bowden, T A" uniqKey="Bowden T" first="T. A." last="Bowden">T. A. Bowden</name><name sortKey="Brown, I H" sort="Brown, I H" uniqKey="Brown I" first="I. H." last="Brown">I. H. Brown</name><name sortKey="Kellam, P" sort="Kellam, P" uniqKey="Kellam P" first="P." last="Kellam">P. Kellam</name><name sortKey="Lam, T T" sort="Lam, T T" uniqKey="Lam T" first="T. T." last="Lam">T. T. Lam</name><name sortKey="Leigh Brown, A J" sort="Leigh Brown, A J" uniqKey="Leigh Brown A" first="A. J." last="Leigh Brown">A. J. Leigh Brown</name><name sortKey="Lycett, S J" sort="Lycett, S J" uniqKey="Lycett S" first="S. J." last="Lycett">S. J. Lycett</name><name sortKey="Pybus, O G" sort="Pybus, O G" uniqKey="Pybus O" first="O. G." last="Pybus">O. G. Pybus</name><name sortKey="Pybus, O G" sort="Pybus, O G" uniqKey="Pybus O" first="O. G." last="Pybus">O. G. Pybus</name><name sortKey="Wood, J L N" sort="Wood, J L N" uniqKey="Wood J" first="J. L. N." last="Wood">J. L. N. Wood</name></country><country name="États-Unis"><region name="Pennsylvanie"><name sortKey="Holmes, E C" sort="Holmes, E C" uniqKey="Holmes E" first="E. C." last="Holmes">E. C. Holmes</name></region><name sortKey="Holmes, E C" sort="Holmes, E C" uniqKey="Holmes E" first="E. C." last="Holmes">E. C. Holmes</name></country><country name="République populaire de Chine"><noRegion><name sortKey="Guan, Y" sort="Guan, Y" uniqKey="Guan Y" first="Y." last="Guan">Y. Guan</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|texte= The evolutionary dynamics of influenza A virus adaptation to mammalian hosts
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