Influenza A Virus Migration and Persistence in North American Wild Birds

Justin Bahl,David E Wentworth,Denise Kühnert,Timothy B Stockwell,Vivien G Dugan,Ian H Mendenhall,Lawrence J Niles,David Walker,Yvonne C F Su,Angela Danner,Alexei J Drummond,Garnet Raven,Mathieu Fourment,Rebecca A Halpin,Scott Krauss,Richard J Webby,S Paul Pryor,Gavin J D Smith,Robert G Webster

doi:10.1371/journal.ppat.1003570

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.

Highlights

Migrating wild birds have been implicated in the spread and emergence of human and livestock influenza, including pandemic influenza and highly pathogenic H5N1 avian influenza [1,2,3]
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
Influenza viruses sampled from Anseriformes in Alberta are representative of the remaining AIV diversity sampled across North America

Summary

Introduction

Migrating wild birds have been implicated in the spread and emergence of human and livestock influenza, including pandemic influenza and highly pathogenic H5N1 avian influenza [1,2,3]. Viral transmission between wild birds and domestic poultry has contributed to genomic reassortment and confounded disease control efforts [2,4]. While it is contentious as to whether wild birds are the primary vectors spreading H5N1 viruses over long distances, there is little doubt that these animals play a role in confounding disease surveillance and control efforts. Even though there is evidence that Anseriformes infected with influenza A virus have hampered migration, these hosts vector influenza viruses vast distances [11,12]. Disease transmissions between the millions of conspecific birds at congregating sites throughout the world contribute to the genetic variability and reassortment of influenza A viruses [13,14]. It is not coincidental that these major breeding, feeding, and staging sites are regions of high viral prevalence [14,15,16,17,18,19,20,21]

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