Contrasting dynamics of two incursions of low-pathogenicity avian influenza virus into Australia

Abstract

The current panzootic of high pathogenicity avian influenza virus H5N1 demonstrates how viral incursions can have major ramifications for wildlife and domestic animals. Herein, we describe the recent incursion into Australia of two low pathogenicity avian influenza virus subtypes, H4 and H10, that exhibited contrasting evolutionary dynamics. Viruses detected from national surveillance and disease investigations between 2020 and 2022 revealed 27 genomes, 24 of which have at least one segment more closely related to Eurasian or North American avian influenza lineages than those already circulating in Australia. Phylogenetic analysis revealed that H4 viruses circulating in shorebirds represent a recent incursion from Asia that is distinct from those circulating concurrently in Australian waterfowl. Analysis of the internal segments further demonstrates exclusive, persistent circulation in shorebirds. This contrasts with H10, where a novel lineage has emerged in wild waterfowl, poultry, and captive birds across Australia and has likely replaced previously circulating H10 lineages through competitive exclusion. Elucidating different dynamics for avian influenza incursions supports effective disease risk identification and communication that better informs disease preparedness and response.

Keywords: H10; H4; LPAI; avian influenza; bird migration; evolution; influenza A virus; low-pathogenicity avian influenza; viral incursion.

Figure 1.

Phylogenetic trees of (a–c) H4 sequences regardless of NA and (d–f) N8 sequences. Phylogenetic trees for the waterfowl clade of H4 and H4-associated NA trees are provided in Supplementary Figs S1 and S2, respectively. (a and d) Maximum likelihood trees comprising all sequences collated for this study. Trees were rooted geographically (i.e. between the ‘Eurasian’ and ‘American’ lineages), and the scale bar corresponds to the number of substitutions per site. (b and e) Time-structured phylogenetic trees. The trees comprise select sequences from relevant lineages (here Eurasian lineages containing Australian sequences). (c and f) Expansion of clade containing Australian sequences of interest, highlighted in a grey box in (b and e). In the case of the HA segment, only the clade containing H4N8 viruses has been highlighted in (c). Sequences of interest are indicated by arrows in (a), (b), (d), and (e) and are highlighted in a box in (c) and (f). Node bars correspond to the 95% HPD of node height. Branches are coloured by continent or are black where geographic origin is ambiguous (i.e. deep branches).

Figure 2.

Phylogenetic trees of all (a–c) H10 sequences regardless of NA and (d–f) N7 sequences. A phylogenetic tree for N2 and N3 is provided in Supplementary Fig. S2. (a and d) Maximum likelihood trees comprising all sequences collated for this study. Trees were rooted geographically (i.e. between the ‘Eurasian’ and ‘American’ lineages), and the scale bar corresponds to the number of substitutions per site. (b and e) Time-structured phylogenetic trees. The trees comprise select sequences from relevant lineages (here Eurasian lineage with all Australian sequences). (c and f), expansion of clade containing Australian sequences of interest, highlighted in a grey box in (b and e). Sequences of interest are indicated by arrows in (a, b, d, and e) and are highlighted in a box in (c and f). Node bars correspond to the 95% HPDof node height. Branches are coloured by continent or are black where geographic origin is ambiguous (i.e. deep branches).