Influenza A Virus Migration and Persistence in North American Wild Birds

Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. T...

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Published in:	PLoS pathogens Vol. 9; no. 8; p. e1003570
Main Authors:	Bahl, Justin, Krauss, Scott, Kühnert, Denise, Fourment, Mathieu, Raven, Garnet, Pryor, S. Paul, Niles, Lawrence J., Danner, Angela, Walker, David, Mendenhall, Ian H., Su, Yvonne C. F., Dugan, Vivien G., Halpin, Rebecca A., Stockwell, Timothy B., Webby, Richard J., Wentworth, David E., Drummond, Alexei J., Smith, Gavin J. D., Webster, Robert G.
Format:	Journal Article
Language:	English
Published:	United States Public Library of Science 01.08.2013 Public Library of Science (PLoS)
Subjects:	Animal Migration Animal populations Animals Avian flu Bird migration Charadriiformes - virology Colleges & universities Confidence intervals Humans Influenza A virus Influenza in Birds - epidemiology Influenza in Birds - transmission Livestock Models, Biological North America - epidemiology Pandemics Trees Viruses North America
ISSN:	1553-7374, 1553-7366, 1553-7374
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Abstract	Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection.
AbstractList	Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection.Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection. Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection. Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection. Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection. Despite continuous virological surveillance (1976–2009) in wild waterfowl (Anseriformes) and shorebirds (Charadriiformes), the ecological and evolutionary dynamics of avian influenza A virus (AIV) in these hosts is poorly understood. Comparative genomic analysis of AIV data revealed that the high prevalence of Charadriiformes infected in Delaware Bay is a reservoir of AIV that is phylogenetically distinct from AIV sampled from most North American Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the remaining AIV diversity sampled across North America. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that this population genetic structure was transient and the long-term persistence of AIV was independent of bird flyways. These results suggest an introduced virus lineage may initially be restricted to one flyway, but migration to a major congregation site such as Alberta could occur followed by subsequent spread across flyways. These generalized predictions for virus movement will be critical to assess the associated risk for widespread diffusion and inform surveillance for pandemic preparedness.
Author	Webster, Robert G. Dugan, Vivien G. Webby, Richard J. Drummond, Alexei J. Walker, David Raven, Garnet Pryor, S. Paul Mendenhall, Ian H. Kühnert, Denise Fourment, Mathieu Su, Yvonne C. F. Halpin, Rebecca A. Stockwell, Timothy B. Bahl, Justin Krauss, Scott Niles, Lawrence J. Wentworth, David E. Smith, Gavin J. D. Danner, Angela
AuthorAffiliation	3 Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, United States of America 6 Environment Canada, Canadian Wildlife Service, Edmonton, Alberta, Canada 9 Division of Microbiology and Infectious Diseases/National Institute of Allergy and Infectious Diseases/National Institutes of Health/Department of Health and Human Services, Bethesda, Maryland, United States of America 10 Duke Global Health Institute, Duke University, Durham, North Carolina, United States of America University of California San Francisco, United States of America 2 Center for Infectious Diseases, The University of Texas School of Public Health, Houston, Texas, United States of America 7 Conserve Wildlife Foundation of New Jersey, Bordentown, New Jersey, United States of America 5 Allan Wilson Centre for Molecular Ecology and Evolution, University of Auckland, Auckland, New Zealand 8 J. Craig Venter Institute, Rockville, Maryland, United States of America 1 Laboratory of Virus Evoluti
AuthorAffiliation_xml	– name: 2 Center for Infectious Diseases, The University of Texas School of Public Health, Houston, Texas, United States of America – name: 7 Conserve Wildlife Foundation of New Jersey, Bordentown, New Jersey, United States of America – name: University of California San Francisco, United States of America – name: 8 J. Craig Venter Institute, Rockville, Maryland, United States of America – name: 6 Environment Canada, Canadian Wildlife Service, Edmonton, Alberta, Canada – name: 3 Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, United States of America – name: 4 Department of Computer Science, University of Auckland, Auckland, New Zealand – name: 10 Duke Global Health Institute, Duke University, Durham, North Carolina, United States of America – name: 1 Laboratory of Virus Evolution, Program in Emerging Infectious Diseases, Duke-NUS Graduate Medical School, Singapore – name: 5 Allan Wilson Centre for Molecular Ecology and Evolution, University of Auckland, Auckland, New Zealand – name: 9 Division of Microbiology and Infectious Diseases/National Institute of Allergy and Infectious Diseases/National Institutes of Health/Department of Health and Human Services, Bethesda, Maryland, United States of America
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Copyright	2013 Bahl et al 2013 Bahl et al 2013 Bahl et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bahl J, Krauss S, Kühnert D, Fourment M, Raven G, et al. (2013) Influenza A Virus Migration and Persistence in North American Wild Birds. PLoS Pathog 9(8): e1003570. doi:10.1371/journal.ppat.1003570
Copyright_xml	– notice: 2013 Bahl et al 2013 Bahl et al – notice: 2013 Bahl et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Bahl J, Krauss S, Kühnert D, Fourment M, Raven G, et al. (2013) Influenza A Virus Migration and Persistence in North American Wild Birds. PLoS Pathog 9(8): e1003570. doi:10.1371/journal.ppat.1003570
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JB SK GJDS RGW. Performed the experiments: JB SK AD DEW DK MF. Analyzed the data: JB AJD DK SK GJDS RGW MF IHM RJW. Contributed reagents/materials/analysis tools: GR SPP LJN YCFS VGD RAH TBS DEW AJD DW. Wrote the paper: JB SK MF IHM AJD DEW GJDS RGW. Programing for joint estimation of migration rates in BEAST: AJD DK. Programming for statistical comparison of tree congruence for assessing reassortment: MF. The authors have declared that no competing interests exist.
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SubjectTerms	Animal Migration Animal populations Animals Avian flu Bird migration Charadriiformes - virology Colleges & universities Confidence intervals Humans Influenza A virus Influenza in Birds - epidemiology Influenza in Birds - transmission Livestock Models, Biological North America - epidemiology Pandemics Trees Viruses
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Title	Influenza A Virus Migration and Persistence in North American Wild Birds
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