Phylogeographic evidence for the inter- and intracontinental dissemination of avian influenza viruses via migration flyways.

Junki Mine,Ivan Sobolev,Alexander Shestopalov,Yuko Uchida,Takehiko Saito,Kirill Sharshov,Charles J Russell

doi:10.1371/journal.pone.0218506

Abstract

Genetically related highly pathogenic avian influenza viruses (HPAIVs) of H5N6 subtype caused outbreaks simultaneously in East Asia and Europe—geographically distinct regions—during winter 2017–2018. This situation prompted us to consider whether the application of phylogeographic analysis to a particular gene segment of AIVs could provide clues for understanding how AIV had been disseminated across the continent. Here, the N6 NA genes of influenza viruses isolated across the world were subjected to phylogeographic analysis to illustrate the inter- and intracontinental dissemination of AIVs. Those isolated in East Asia during winter and in Mongolia/Siberia during summer were comingled within particular clades of the phylogeographic tree. For AIVs in one clade, their dissemination in eastern Eurasia extended from Yakutia, Russia, in the north to East Asia in the south. AIVs in western Asia, Europe, and Mongolia were also comingled within other clades, indicating that Mongolia/Siberia plays an important role in the dissemination of AIVs across the Eurasian continent. Mongolia/Siberia may therefore have played a role in the simultaneous outbreaks of H5N6 HPAIVs in Europe and East Asia during the winter of 2017–2018. In addition to the long-distance intracontinental disseminations described above, intercontinental disseminations of AIVs between Eurasia and Africa and between Eurasia and North America were also observed. Integrating these results and known migration flyways suggested that the migration of wild birds and the overlap of flyways, such as that observed in Mongolia/Siberia and along the Alaskan Peninsula, contributed to the long-distance intra- and intercontinental dissemination of AIVs. These findings highlight the importance of understanding the movement of migratory birds and the dynamics of AIVs in breeding areas—especially where several migration flyways overlap—in forecasting outbreaks caused by HPAIVs.

Highlights

Influenza A viruses have been isolated from birds and from various mammals, including pigs and humans [1]
By applying the criteria of the clade definition of H5 HA genes of Eurasian highly pathogenic avian influenza viruses (HPAIVs) [45], eight and 25 clades that consisted of at least five strains were recognized in the North American and Eurasian lineages, respectively (Figs 1 and 2, S1–S7 Figs)
N6 NA genes of the H5N6 HPAIVs isolated in Asia and Europe during the winter of 2017– 2018 were categorized into two clades, A and B (Fig 3a, S1 Fig), in the Eurasian lineage

Summary

Introduction

Influenza A viruses have been isolated from birds and from various mammals, including pigs and humans [1]. Some studies suggested that the movement of migratory birds from Asian wintering sites to breeding sites in Far East Siberia and the Alaskan Peninsula, and the subsequent southward movement along the Pacific coast of North America, could be related to this spread of HPAIVs [27, 28]. A previous report demonstrated that H5 HPAIVs, which showed high pathogenicity in poultry under experimental infection, caused mild or no clinical signs in wild birds [29]. These events highlight the involvement of wild birds in the spread of AIVs, including HPAIVs [30]

Methods

Results

Discussion

Conclusion