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Title: Influenza A Virus Migration and Persistence in North American Wild Birds}
Article:
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.
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]–[3]. Viral transmission between wild birds and domestic poultry has contributed to genomic reassortment and confounded disease control efforts[2],[4]. Subsequently, with the reintroduction of H5N1 to wild birds the virus has spread throughout Eurasia and Africa[5]–[9]. 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. It is estimated worldwide that over 50 billion birds migrate annually between breeding and non-breeding areas[10]. 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 also regions of high viral prevalence[14]–[21]. Recent efforts to assess invasive virological threats have focused on increased surveillance and early detection of introduced viral strains[22]–[24]. Influenza A viruses have transmitted between the Eurasian and North American wild Anseriformes and Charadriformes gene pools where birds from both continental regions commingle and therefore the threat posed by introduction of H5N1 to North America remains. However, once a virological threat has entered the North American bird population there is little information regarding how that virus may behave or diffuse between spatially distant migratory bird populations. The prediction of viral spread and disease emergence, as well as formulation of preparedness plans has generally been based on ad hoc approaches. This is largely due to a critical lack of knowledge of viral movements between different host populations[13]–[17]. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Methodological advances present an opportunity for large-scale assessment of spatiotemporal patterns of viral movement between migrating bird populations. In this study we identified 20 discrete regions in North America where influenza viruses have been systematically collected from wild birds to determine whether the viral population was structured according to host migratory flyways, and rates of gene flow between these populations. Avian influenza viruses were isolated annually throughout our surveillance in Alberta, Canada and Delaware Bay, USA and an additional 287 genomes were sequenced. Using full genome data we characterize the reassortment dynamics, spatial diffusion patterns and evolutionary genomics of influenza A viruses in North America collected over a 25-year period from migratory birds.
Discussion:
Our goal was to understand the migration dynamics and diffusion patterns of influenza virus in their natural hosts by utilizing over 30 years of continuous systematic surveillance data. We show that our surveillance within Alberta, which includes convergence points for all four migratory flyways[28],[29], is capturing the majority of genetic diversity of the North American influenza gene pool. Breeding birds converging in this region facilitate the spread and generation of influenza virus genetic diversity indicating the importance of Anseriformes' social behavior in persistence of the virus population. The site at Delaware Bay has been identified as a hotspot for avian influenza A viruses[30], where hundreds of thousands of migrating Charadriiformes stopover annually to feed in highly dense congregations. Our results showed limited genetic diversity coupled with high prevalence of infection indicating an epizootic in Charadriiformes that does not play a significant role in the shaping the sampled AIV diversity within North American Anseriformes. Even though this hotspot is not representative of gene pool diversity, these viruses are ultimately derived from the same population of viruses common throughout North America. The transmission of viruses between populations of birds is most likely occurring where migratory Anseriformes and Charadriiformes commingle, possibly in South and Central America or Arctic breeding grounds. The role of Charadriiformes in the persistence and transmission of influenza A viruses therefore warrants further study, especially on a more comprehensive spatial scale. We show that the long-term persistence of the influenza A virus gene pool in North American wild birds may be independent of migratory flyways. Although virus migration could be restricted within a flyway over short time periods, our results show strong support for longer-term lateral diffusion of viral lineages between host populations. In our study, data points were not assigned to a flyway but discrete sites were assigned and used to inform within and between flyway migration rates using tip-dated time-dependent phylogenetic reconstructions. While this does contradict previous work by Lam et al[27], which suggested that migratory flyways and distance might represent a barrier for migration, both studies show that migration between flyways does occur[27]. Our study shows that the short-term evolutionary consequences of these ecological barriers may be rapidly erased by East-West virus migration, and that such diffusion may be critical for the survival and persistence of novel virus lineages introduced to North American wild birds. Subtype specific host distribution, geographic state definition and host ecology may also be a source for the differences observed between the two studies[27]. While we found no correlation between distance migrated and rate of migration, analysis of the H3-HA indicated that subtype specific diffusion patterns might be different. In turn this may be related to host specificity of H3 viruses. Furthermore, in our study we cannot detect migration events where the distance migrated is less than 400 km due to the definition we used for geographic states( 5′×5′ latitude-longitude square). The data used in our analysis included collections from resident and short distance migratory birds[31]. This data was unavailable to Lam et al[27], and may further account for the observed differences. In our study we assume that virus migration was the same regardless of host. This assumption may be valid when analyzing viruses from all hosts in a single analysis, it is unlikely to be justified when considering specific hosts. Flyways are often applied universally to all hosts, whereas there are clear differences in the behavior and ecological habits of different hosts( see supporting information Text S1). Using our model for virus transmission generalized predictions for movement of an introduced Eurasian virus and the associated risk for widespread diffusion can be inferred. An introduced virus lineage to Alaska might initially be restricted to the Pacific Flyway, but migration to a major congregation site such as Alberta could occur with subsequent spread across flyways occurring shortly after. While the establishment of introduced lineages into North America may be rare, introduction and reassortment events with Eurasian and North American strains probably occur more frequently than detected[16],[17],[32]. The development of fully resolved ecological and viral risk models depend upon the continued long-term active surveillance in major bird congregation zones. While the resolution and detection of migration events has been enhanced with increased surveillance in recent years, critical information for wild bird surveillance remains sparse. This is especially evident as no sampling in Central and South America was available for this study. A comprehensive understanding of spatial diffusion patterns of viruses introduced to wild animal populations is critical for the development of preparedness plans in response to emerging viral threats.
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 .