Phylogenetic Analysis Reveals the Global Migration of Seasonal Influenza A Viruses

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Abstract
The winter seasonality of influenza A virus in temperate climates is one of the most widely recognized, yet least understood, epidemiological patterns in infectious disease. Central to understanding what drives the seasonal emergence of this important human pathogen is determining what becomes of the virus during the non-epidemic summer months. Herein, we take a step towards elucidating the seasonal emergence of influenza virus by determining the evolutionary relationship between populations of influenza A virus sampled from opposite hemispheres. We conducted a phylogenetic analysis of 487 complete genomes of human influenza A/H3N2 viruses collected between 1999 and 2005 from Australia and New Zealand in the southern hemisphere, and a representative sub-sample of viral genome sequences from 413 isolates collected in New York state, United States, representing the northern hemisphere. We show that even in areas as relatively geographically isolated as New Zealand's South Island and Western Australia, global viral migration contributes significantly to the seasonal emergence of influenza A epidemics, and that this migration has no clear directional pattern. These observations run counter to suggestions that local epidemics are triggered by the climate-driven reactivation of influenza viruses that remain latent within hosts between seasons or transmit at low efficiency between seasons. However, a complete understanding of the seasonal movements of influenza A virus will require greatly expanded global surveillance, particularly of tropical regions where the virus circulates year-round, and during non-epidemic periods in temperate climate areas. The winter seasonality of influenza A virus in temperate climates is one of the most puzzling epidemiological patterns in infectious disease. To help resolve the issue of influenza seasonality, we studied, using viral genome sequence data, the patterns of global migration of influenza A virus, particularly between the northern and southern hemispheres. A phylogenetic analysis of approximately 900 complete genomes of the H3N2 subtype of human influenza A virus sampled from New Zealand and Australia (southern hemisphere), and New York state, United States (northern hemisphere), revealed that cross-hemisphere migration frequently occurs in both directions and involves multiple viral strains. Such global viral traffic therefore contributes significantly to the introduction of new influenza epidemics in both northern and southern hemispheres. These results also show that influenza A virus migrates afar during non-epidemic periods, rather than persisting locally at low levels during the influenza “off-season”. However, although this represents the largest and first bihemisphere study of its kind to our knowledge, the results highlight the need for sampling from tropical regions and during non-epidemic periods in temperate areas. Studies of this kind are critical to fully understand the geographical dispersal of influenza A virus and the role of climate in triggering seasonal epidemics.