Avian influenza H5N1 viral and bird migration networks in Asia

Abstract

The spatial spread of the highly pathogenic avian influenza virus H5N1 and its long-term persistence in Asia have resulted in avian influenza panzootics and enormous economic losses in the poultry sector. However, an understanding of the regional long-distance transmission and seasonal patterns of the virus is still lacking. In this study, we present a phylogeographic approach to reconstruct the viral migration network. We show that within each wild fowl migratory flyway, the timing of H5N1 outbreaks and viral migrations are closely associated, but little viral transmission was observed between the flyways. The bird migration network is shown to better reflect the observed viral gene sequence data than other networks and contributes to seasonal H5N1 epidemics in local regions and its large-scale transmission along flyways. These findings have potentially far-reaching consequences, improving our understanding of how bird migration drives the periodic reemergence of H5N1 in Asia.

Keywords: HPAI H5N1; bird migration; network; satellite tracking; viral migration.

Fig. 1.

Research regions, bird migration routes, and phylogeny of the clade 2.3.2 HPAI H5N1 virus samples based on the sequences of the HA gene. (A) Central Asian (CA) and East Asian–Australasian (EA) flyways of the bar-headed goose, swan goose, ruddy shelduck, and northern pintail, monitored with satellite telemetry over the period 2006–2009. (B) Geographic distribution of outbreaks (red spots) and viral samples (colored squares), according to region. (C) Temporally structured maximum clade credibility phylogenetic tree of the HA gene. Branches are colored according to geographic regions.

Fig. 2.

Temporal relationships between H5N1 outbreaks and bird migration along flyways in Asia. (A) Scatterplot of the mean annual lags between epidemics against average flight time during the migration between regions of four bird species: bar-headed goose (Anser indicus), swan goose (Anser cygnoides), ruddy shelduck (Tadorna ferruginea), and northern pintail (Anas acuta) between regions. The lines correspond to the linear regression based on the circles indicated by the two flyways (green: East Asian–Australasian flyway, EA flyway; red: Central Asian flyway, CA flyway). (B) Epidemic velocity against bird migration speed along the EA flyway and (C) CA flyway.

Fig. 3.

Viral migration and bird migration networks in Asia. (A) Supported state transitions of HPAI H5N1 clades 2.3.2. (B) The migration routes of the four main bird species [bar-headed goose (Anser indicus), swan goose (Anser cygnoides), ruddy shelduck (Tadorna ferruginea), and northern pintail (Anas acuta)] in the Central Asian (CA, red line), East Asian–Australasian 1 (EA-1, starting at Hong Kong, green line), and East Asian–Australasian 2 flyways (EA-2, starting at Poyang Lake, dark green line).

Fig. 4.

Viral gene flow and bird migration network. (A) The bird migration network along the East Asian–Australasian 1 flyway (EA-1, starting at Hong Kong), and the associated partial phylogeny describing the relationship with the viral strains from Japan and Zhejiang Province. (B) Example of randomly generated viral migration networks. Viral migration was assumed to follow an underlying migration process along an unobserved network. A total of 1,000 random networks were created in each flyway. (C) Migration history tests were implemented by measuring spatial distances together with the migration history (blue line) or without the migration history (direct spatial distance measurement from Japan to Zhejiang, black line). The hexagon and edges represent the possible network graph of the locations (nodes) in the flyway. The migration routes are illustrated by blue lines.

Fig. 5.

Correlation of the gene flow network with randomly generated networks of HPAI H5N1 clade 2.3.2. (A) Histogram of the correlation coefficients; blue bars represent the purely random network model, cyan bars represent the random categorized network model, and gray bars are flyway-based random networks. (B) Histogram of the correlation coefficients for the flyway-based random networks and bird migration networks: green, East Asian–Australasian 1 flyway (starting at Hong Kong); dark green, East Asian–Australasian 2 flyway (starting at Poyang Lake); and red, Central Asian flyway. Each test is based on 1,000 random networks. (C) Correlation coefficients for each flyway-based network against the total perimeter of the network. Box indicates the maximum and minimum range; black point represents the median.