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Australia as a global sink for the genetic diversity of avian influenza A virus

View ORCID ProfileMichelle Wille, Victoria (Tiggy) Grillo, Silvia Ban de Gouvea Pedroso, Graham W. Burgess, Allison Crawley, Celia Dickason, Philip M. Hansbro, Md. Ahasanul Hoque, Paul F Horwood, Peter D Kirkland, Nina Yu-Hsin Kung, Stacey E. Lynch, Sue Martin, Michaela McArthur, Kim O’Riley, Andrew J Read, Simone Warner, Bethany J. Hoye, Simeon Lisovski, Trent Leen, Aeron C. Hurt, Jeff Butler, Ivano Broz, Kelly R. Davies, Patrick Mileto, Matthew Neave, Vicky Stevens, Andrew Breed, Tommy T. Y. Lam, Edward C. Holmes, Marcel Klaassen, Frank Y. K. Wong
doi: https://doi.org/10.1101/2021.11.30.470533
Michelle Wille
1WHO Collaborating Centre for Reference and Research on Influenza, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
2Sydney Institute for Infectious Diseases, School of Life and Environmental Sciences and School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia
3Department of Microbiology and Immunology, at the Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, Victoria, Australia
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  • ORCID record for Michelle Wille
  • For correspondence: michelle.wille@sydney.edu.au Frank.Wong@csiro.au
Victoria (Tiggy) Grillo
4Wildlife Health Australia, Mosman, New South Wales, Australia
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Silvia Ban de Gouvea Pedroso
4Wildlife Health Australia, Mosman, New South Wales, Australia
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Graham W. Burgess
5College of Public Health, Medical and Veterinary Sciences, James Cook University, Townville, Queensland, Australia
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Allison Crawley
6Primary Industries and Regions, Adelaide, South Australia, Australia
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Celia Dickason
6Primary Industries and Regions, Adelaide, South Australia, Australia
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Philip M. Hansbro
7Centre for Inflammation, Centenary Institute and University of Technology Sydney, School of Life Sciences, Faculty of Science, Sydney NSW, Australia
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Md. Ahasanul Hoque
8Chattogram (previously Chittagong) Veterinary and Animal Sciences University, Khulshi, Bangladesh
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Paul F Horwood
5College of Public Health, Medical and Veterinary Sciences, James Cook University, Townville, Queensland, Australia
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Peter D Kirkland
9NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, New South Wales, Australia
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Nina Yu-Hsin Kung
10Animal Biosecurity & Welfare, Biosecurity Queensland, Department of Agriculture and Fisheries, Health Food Science Precinct, Coopers Plains, Queensland, Australia
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Stacey E. Lynch
11Agriculture Victoria Research, AgriBio Centre for AgriBioscience, Bundoora, Victoria, Australia
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Sue Martin
12Department of Primary Industries, Parks, Water and Environment, Tasmania, Australia
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Michaela McArthur
13Department of Primary Industries and Regional Development, Western Australia, Australia
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Kim O’Riley
11Agriculture Victoria Research, AgriBio Centre for AgriBioscience, Bundoora, Victoria, Australia
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Andrew J Read
9NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Menangle, New South Wales, Australia
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Simone Warner
11Agriculture Victoria Research, AgriBio Centre for AgriBioscience, Bundoora, Victoria, Australia
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Bethany J. Hoye
14Centre for Integrative Ecology, Deakin University, Geelong, Victoria, Australia
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Simeon Lisovski
14Centre for Integrative Ecology, Deakin University, Geelong, Victoria, Australia
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Trent Leen
15Geelong Field & Game, Geelong, Victoria, Australia
16Wetlands Environmental Taskforce. Field & Game Australia, Seymour, Victoria, Australia
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Aeron C. Hurt
1WHO Collaborating Centre for Reference and Research on Influenza, at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
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Jeff Butler
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Ivano Broz
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Kelly R. Davies
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Patrick Mileto
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Matthew Neave
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Vicky Stevens
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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Andrew Breed
18Department of Agriculture, Water and the Environment, Canberra, Australian Capital Territory, Australia
19University of Queensland, St. Lucia, Queensland, Australia
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Tommy T. Y. Lam
20State Key Laboratory of Emerging Infectious Diseases, School of Public Health, The University of Hong Kong, Hong Kong, PR China
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Edward C. Holmes
2Sydney Institute for Infectious Diseases, School of Life and Environmental Sciences and School of Medical Sciences, The University of Sydney, Sydney, New South Wales, Australia
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Marcel Klaassen
14Centre for Integrative Ecology, Deakin University, Geelong, Victoria, Australia
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Frank Y. K. Wong
17Commonwealth Scientific and Industrial Research Organisation (CSIRO), Australian Centre for Disease Preparedness, Geelong, Victoria, Australia
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  • For correspondence: michelle.wille@sydney.edu.au Frank.Wong@csiro.au
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Abstract

Most of our understanding of the ecology and evolution of avian influenza A virus (AIV) in wild birds is derived from studies conducted in the northern hemisphere on waterfowl, with a substantial bias towards dabbling ducks. However, relevant environmental conditions and patterns of avian migration and reproduction are substantially different in the southern hemisphere. Through the sequencing and analysis of 333 unique AIV genomes collected from wild birds collected over 15 years we show that Australia is a global sink for AIV diversity and not integrally linked with the Eurasian gene pool. Rather, AIV are infrequently introduced to Australia, followed by decades of isolated circulation and eventual extinction. The number of co-circulating viral lineages varies per subtype. AIV haemagglutinin (HA) subtypes that are rarely identified at duck-centric study sites (H8-12) had more detected introductions and contemporary co-circulating lineages in Australia. Combined with a lack of duck migration beyond the Australian-Papuan region, these findings suggest introductions by long-distance migratory shorebirds. In addition, we found no evidence of directional or consistent patterns in virus movement across the Australian continent. This feature corresponds to patterns of bird movement, whereby waterfowl have nomadic and erratic rainfall-dependant distributions rather than consistent intra-continental migratory routes. Finally, we detected high levels of virus gene segment reassortment, with a high diversity of AIV genome constellations across years and locations. These data, in addition to those from other studies in Africa and South America, clearly show that patterns of AIV dynamics in the Southern Hemisphere are distinct from those in the temperate north.

Author Summary A result of the ever-growing poultry industry is a dramatic global increase in the incidence of high pathogenicity avian influenza virus outbreaks. In contrast, wild birds are believed to be the main reservoir for low pathogenic avian influenza A virus. Due to intensive research and surveillance of AIV in waterfowl in the Northern Hemisphere, we have a better understanding of AIV ecology and evolution in that region compared to the Southern Hemisphere, which are characterised by different patterns of avian migration and ecological conditions. We analysed 333 unique AIV genomes collected from wild birds in Australia to understand how Australia fits into global AIV dynamics and how viruses are maintained and dispersed within the continent of Australia. We show that the Southern Hemisphere experiences differing evolutionary dynamics to those seen in Northern Hemisphere with Australia representing a global sink for AIV.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Australia as a global sink for the genetic diversity of avian influenza A virus
Michelle Wille, Victoria (Tiggy) Grillo, Silvia Ban de Gouvea Pedroso, Graham W. Burgess, Allison Crawley, Celia Dickason, Philip M. Hansbro, Md. Ahasanul Hoque, Paul F Horwood, Peter D Kirkland, Nina Yu-Hsin Kung, Stacey E. Lynch, Sue Martin, Michaela McArthur, Kim O’Riley, Andrew J Read, Simone Warner, Bethany J. Hoye, Simeon Lisovski, Trent Leen, Aeron C. Hurt, Jeff Butler, Ivano Broz, Kelly R. Davies, Patrick Mileto, Matthew Neave, Vicky Stevens, Andrew Breed, Tommy T. Y. Lam, Edward C. Holmes, Marcel Klaassen, Frank Y. K. Wong
bioRxiv 2021.11.30.470533; doi: https://doi.org/10.1101/2021.11.30.470533
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Australia as a global sink for the genetic diversity of avian influenza A virus
Michelle Wille, Victoria (Tiggy) Grillo, Silvia Ban de Gouvea Pedroso, Graham W. Burgess, Allison Crawley, Celia Dickason, Philip M. Hansbro, Md. Ahasanul Hoque, Paul F Horwood, Peter D Kirkland, Nina Yu-Hsin Kung, Stacey E. Lynch, Sue Martin, Michaela McArthur, Kim O’Riley, Andrew J Read, Simone Warner, Bethany J. Hoye, Simeon Lisovski, Trent Leen, Aeron C. Hurt, Jeff Butler, Ivano Broz, Kelly R. Davies, Patrick Mileto, Matthew Neave, Vicky Stevens, Andrew Breed, Tommy T. Y. Lam, Edward C. Holmes, Marcel Klaassen, Frank Y. K. Wong
bioRxiv 2021.11.30.470533; doi: https://doi.org/10.1101/2021.11.30.470533

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