Influenza a virus migration and persistence in North American wild birds

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.

Figure 1. A) H3-HA phylogenetic tree for isolates from Alberta.

B) H3-HA phylogenetic tree for isolates from Delaware Bay. C) H3-HA phylogenetic tree for isolates from Alaska. D) Multidimensional scaling of tree-to-tree TMRCA estimates from Alberta. For reference, the space occupied by human H3N2 viruses from similar analysis is centered (grey circle). E) Multidimensional scaling of tree-to-tree patristic distance from Delaware Bay. F) Multidimensional scaling of tree-to-tree patristic distance from Alaska.

Figure 2. Bayesian relaxed clock HA gene phylogenetic tree from all H3 wild bird isolates in North America.

The two co-circulating North American lineages (I and II) are annotated to the right of the tree. Branches are colored according to ancestral state location estimated from geographical tip-state observations for all observed localities.

Figure 3. A) Mean migration rate per MCMC step within flyway migration rates vs Mean between flyway migration jointly estimated from all publically available PA, PB1, PB2, NP and M gene segments.

B) Density distribution of mean within flyway and mean between flyway rates.

Figure 4. Patterns of viral migration jointly estimated across the 5 internal protein gene segments.

Lines connecting discrete regions indicate statistically supported ancestral state changes and are thickened according to statistical support. There are five categories of support. The thinnest lines indicate 6≤BF<10 (supported); 10≤BF<30 (strong support); 30≤BF<100 (very strong support) and the thickest lines with BF≤100 (decisive support). Dashed lines indicate statistical supports between 3≤BF<6 but with posterior probabilities <0.5.