Ecological divergence of wild birds drives avian influenza spillover and global spread

Abstract

The diversity of influenza A viruses (IAV) is primarily hosted by two highly divergent avian orders: Anseriformes (ducks, swans and geese) and Charadriiformes (gulls, terns and shorebirds). Studies of IAV have historically focused on Anseriformes, specifically dabbling ducks, overlooking the diversity of hosts in nature, including gull and goose species that have successfully adapted to human habitats. This study sought to address this imbalance by characterizing spillover dynamics and global transmission patterns of IAV over 10 years at greater taxonomic resolution than previously considered. Furthermore, the circulation of viral subtypes in birds that are either host-adapted (low pathogenic H13, H16) or host-generalist (highly pathogenic avian influenza—HPAI H5) provided a unique opportunity to test and extend models of viral evolution. Using Bayesian phylodynamic modelling we uncovered a complex transmission network that relied on ecologically divergent bird hosts. The generalist subtype, HPAI H5 was driven largely by wild geese and swans that acted as a source for wild ducks, gulls, land birds, and domestic geese. Gulls were responsible for moving HPAI H5 more rapidly than any other host, a finding that may reflect their long-distance, pelagic movements and their immuno-naïve status against this subtype. Wild ducks, long viewed as primary hosts for spillover, occupied an optimal space for viral transmission, contributing to geographic expansion and rapid dispersal of HPAI H5. Evidence of inter-hemispheric dispersal via both the Pacific and Atlantic Rims was detected, supporting surveillance at high latitudes along continental margins to achieve early detection. Both neutral (geographic expansion) and non-neutral (antigenic selection) evolutionary processes were found to shape subtype evolution which manifested as unique geographic hotspots for each subtype at the global scale. This study reveals how a diversity of avian hosts contribute to viral spread and spillover with the potential to improve surveillance in an era of rapid global change.

Outbreak of Highly Pathogenic Avian Influenza H5N1 in New England Seals

“…Migratory waterfowl are natural reservoirs for influenza A viruses, allowing long range and transcontinental movement of these viruses (26). Marine mammals are known to be susceptible to a wide range of influenza subtypes that can cause large scale mortality events, or asymptomatic circulation within the population (6).…”

Genetic Analysis of a Novel H16N3 Virus Isolated from a Migratory Gull in China in 2021 and Animal Studies of Infection

“…The introduction of avian influenza viruses of wild bird origin into domestic waterfowl and poultry populations will increase epidemic risks due to replication and transmissibility alterations ( 11 , 17 – 19 ). However, the infectivity and replication properties of the currently circulating H16N3 viruses have not been fully investigated.…”

Ecogeographic drivers of the spatial spread of highly pathogenic avian influenza outbreaks in Europe and North America, 2016-2022

“…There are roughly four times as many individual species of birds in North America as compared with Europe (2059 species versus 544 species) [59,60]. While evidence is lacking with respect to the relationship between avian species diversity and IAV spread, recent data have demonstrated that transmission relies on ecologically divergent bird hosts, and taxonomic diversity is associated with differences in H5N1-associated wild bird mortality due between Europe and Asia [61,62]. Increased virus diffusion when viruses transition to US regions may also relate to relative immune-naivety of avian species in North America versus Europe, given that H5Nx HPAI viruses did not circulate in the North American region for approximately 6 years between 2015 and 2021 [1].…”