Evolutionary features of a prolific subtype of avian influenza: A virus in European waterfowl

Michelle Wille, Conny Tolf, Neus Latorre-Margalef, Ron A. M. Fouchier, Rebecca A. Halpin, David E. Wentworth, Jayna Ragwani, Oliver G. Pybus, Bjorn Olsen, Jonas Waldenstrom

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Abstract

Avian influenza A virus (AIV) is ubiquitous in waterfowl and is detected annually at high prevalence in waterfowl during the Northern Hemisphere autumn. Some AIV subtypes are globally common in waterfowl, such as H3N8, H4N6, and H6N2, and are detected in the same populations at a high frequency, annually. In order to investigate genetic features associated to the long-term maintenance of common subtypes in migratory ducks, we sequenced 248 H4 viruses isolated across 8 years (2002-9) from mallards (Anas platyrhynchos) sampled in southeast Sweden. Phylogenetic analyses showed that both H4 and N6 sequences fell into three distinct lineages, structured by year of isolation. Specifically, across the 8 years of the study, we observed lineage replacement, whereby a different HA lineage circulated in the population each year. Analysis of deduced amino acid sequences of the HA lineages illustrated key differences in regions of the globular head of hemagglutinin that overlap with established antigenic sites in homologous hemagglutinin H3, suggesting the possibility of antigenic differences among these HA lineages. Beyond HA, lineage replacement was common to all segments, such that novel genome constellations were detected across years. A dominant genome constellation would rapidly amplify in the duck population, followed by unlinking of gene segments as a result of reassortment within 2-3 weeks following introduction. These data help reveal the evolutionary dynamics exhibited by AIV on both annual and decadal scales in an important reservoir host.

Original languageEnglish
Article number074
Number of pages11
JournalVirus Evolution
Volume8
Issue number2
Early online date27 Aug 2022
DOIs
Publication statusPublished - 15 Sept 2022

Bibliographical note

Funding Information:
We thank all the staff at Ottenby Bird Observatory for trapping and sampling mallards, and all laboratory staff for processing samples over the years. This is manuscript 325 from Ottenby Bird Observatory. This study was supported by grants from the Swedish Environmental Protection Agency (V-124-01 and V-98-04), the Swedish Research Council VR (2008-58, 2010-3067, and 2011-48), the Swedish Research Council Formas (2007-297 and 2009-1220), and the Sparbanksstiftelsen Kronan. The surveillance at Ottenby was part of the European Union wild bird surveillance and has received support from the Swedish Board of Agriculture and from the EU FP6-funded New Flubird project. Sequencing has been funded in whole or part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services under Contract Number HHSN272200900007C. M.W. was supported by a PGS-D2 from the Natural Sciences and Engineering Research Council (2011–13) and is currently supported by an Australian Research Council Discovery Early Career Research Award (DE200100977). O.G.P. and J.R. were supported by the GCRF One Health Poultry Hub (Grant No. BB/S011269/1). This manuscript was prepared while DEW was employed at the J. Craig Venter Institute. The opinions expressed in this article are the author’s own and do not reflect the view of the Centers for Disease Control, the Department of Health and Human Services, or the US government.

Publisher Copyright:
© The Author(s) 2022. Published by Oxford University Press.

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