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Viruses on the wing: evolution and dynamics of influenza A virus in the Mallard reservoir
Linnaeus University, Faculty of Health and Life Sciences, Department of Biology and Environmental Science. (Zoonotic Ecology, EEMiS)ORCID iD: 0000-0002-5629-0196
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

This thesis explores the evolution of avian influenza A viruses (IAV), as well as host-pathogen interactions between these viruses and their main reservoir host, the Mallard (Anas platyrhynchos). IAV is a genetically diverse, multi-host virus and wild birds, particularly dabbling ducks, are the natural reservoir. At our study site, up to 30% of migratory Mallards are infected with IAV during an autumn season, and host a large number of virus subtypes. IAV diversity is driven by two main mechanisms: mutation, driving genetic drift; and reassortment following co-infection, resulting in genetic shift.

 

Reassortment is pervasive within an autumn season, both across multiple subtypes and within a single subtype. It is a key genetic feature in long-term maintenance of common subtypes, as it allows for independent lineage turn-over, generating novel genetic constellations. I hypothesize that the decoupling of successful constellations and generation of novel annual constellations enables viruses to escape herd immunity; these genetic changes must confer antigenic change for the process to be favourable. Indeed, in an experiment utilizing vaccines, circulating viruses escaped homosubtypic immunity, resulting in the proliferation of infections with the same subtype as the vaccine. While the host plays an important role in shaping IAV evolutionary genetics, one must consider that Mallards are infected with a multitude of other microorganisms. Here, Mallards were infected with IAV, gamma coronaviruses, and avian paramyxovirus type 1 simultaneously, and we found a putative synergistic interaction between IAV and gamma coronaviruses.

 

Mallards occupy the interface between humans, poultry, and wild birds, and are the reservoir of IAV diversity. New incursions of highly pathogenic H5 viruses to both Europe and North America reaffirms the role of wild birds, particularly waterfowl, in diffusion of viruses spatially. Using European low pathogenic viruses and Mallard model, this thesis contributes to aspects of epidemiology, ecology, and evolutionary dynamics of waterfowl viruses, particularly IAV

Place, publisher, year, edition, pages
Växjö: Linnaeus University Press, 2015.
Series
Linnaeus University Dissertations ; 217/2015
Keyword [en]
Co-infections, Ecology, Epidemiology, Evolution, Host-Parasite Interactions, Immunity, Influenza A Virus, Mallard, Phylogeny, Virology, Waterfowl, Wild Birds, Wildlife Disease
National Category
Ecology
Research subject
Natural Science, Zoonotic Ecology
Identifiers
URN: urn:nbn:se:lnu:diva-41431ISBN: 978-91-87925-56-6 (print)OAI: oai:DiVA.org:lnu-41431DiVA, id: diva2:798569
Public defence
2015-05-08, Fullriggaren, Landgången 4, Kalmar, 09:30 (English)
Opponent
Supervisors
Available from: 2015-03-27 Created: 2015-03-27 Last updated: 2015-12-04Bibliographically approved
List of papers
1. Frequency and patterns of reassortment in natural influenza A virus infection in a reservoir host
Open this publication in new window or tab >>Frequency and patterns of reassortment in natural influenza A virus infection in a reservoir host
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2013 (English)In: Virology, ISSN 0042-6822, E-ISSN 1096-0341, Vol. 443, no 15, p. 150-160Article in journal (Refereed) Published
Abstract [en]

Influenza A viruses (IAV) can dramatically alter both genotype and phenotype at a rapid rate as a product of co-infection and reassortment Avian IAV exhibit high levels of phylogenetic incongruence, suggesting high levels of reassortment in the virus reservoir. Using a natural-experimental system, we reconstructed relationships amongst 92 viruses across 15 subtypes from 10 Mallards in an autumn season. Phylogenetic analyses estimated that 56% of the isolated viruses were reassorted. Network analysis demonstrated different patterns of reassortment and limited exchange of segments between primary and secondary infections. No clear patterns of linkage between segments were found, and patterns within a season were likely the consequence of continued introduction ofnew constellations, high viral load and diversity in the wild bird reservoir, and co-infections. This is the first IAV study to implement multiple tools available for elucidating factors governing reassortment patterns in naturally infected Mallards.

National Category
Microbiology
Research subject
Natural Science, Microbiology
Identifiers
urn:nbn:se:lnu:diva-32897 (URN)10.1016/j.virol.2013.05.004 (DOI)000322289900017 ()2-s2.0-84879784330 (Scopus ID)
Available from: 2014-03-17 Created: 2014-03-17 Last updated: 2017-12-05Bibliographically approved
2. Limited diffusion of genome constellations and pervasive reassortment arefeatures of long-term circulation of H4N6 influenza A in European waterfowl
Open this publication in new window or tab >>Limited diffusion of genome constellations and pervasive reassortment arefeatures of long-term circulation of H4N6 influenza A in European waterfowl
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(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Research subject
Natural Science, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-42277 (URN)
Available from: 2015-04-14 Created: 2015-04-14 Last updated: 2015-12-04Bibliographically approved
3. Putative escape and poor humoral response to inactivatedvaccine in Mallards results in no homo- or heterosubtypic immunity againstH3 influenza A in a natural-experimental system.
Open this publication in new window or tab >>Putative escape and poor humoral response to inactivatedvaccine in Mallards results in no homo- or heterosubtypic immunity againstH3 influenza A in a natural-experimental system.
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(English)Manuscript (preprint) (Other academic)
National Category
Biological Sciences
Research subject
Natural Science, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-42278 (URN)
Available from: 2015-04-14 Created: 2015-04-14 Last updated: 2015-12-04Bibliographically approved
4. Temporal dynamics, diversity, and interplay in three components of the virodiversity of a Mallard population: Influenza A virus, avian paramyxovirus and avian coronavirus
Open this publication in new window or tab >>Temporal dynamics, diversity, and interplay in three components of the virodiversity of a Mallard population: Influenza A virus, avian paramyxovirus and avian coronavirus
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2015 (English)In: Infection, Genetics and Evolution, ISSN 1567-1348, E-ISSN 1567-7257, Vol. 29, p. 129-137Article in journal (Refereed) Published
Abstract [en]

Multiple infections, or simultaneous infection of a host with multiple parasites, are the rule rather than the exception. Interactions between co-occurring pathogens in a population may be mutualistic, competitive or facilitative. For some pathogen combinations, these interrelated effects will have epidemiological consequences; however this is as yet poorly incorporated into practical disease ecology. For example, screening of Mallards for influenza A viruses (IAV) have repeatedly revealed high prevalence and large subtype diversity in the Northern Hemisphere. Other studies have identified avian paramyxovirus type 1 (APMV-1) and coronaviruses (CoVs) in Mallards, but without making inferences on the larger viral assemblage. In this study we followed 144 wild Mallards across an autumn season in a natural stopover site and constructed infection histories of IAV, APMV-1 and CoV. There was a high prevalence of IAV, comprising of 27 subtype combinations, while APMV-1 had a comparatively low prevalence (with a peak of 2%) and limited strain variation, similar to previous findings. Avian CoVs were common, with prevalence up to 12%, and sequence analysis identified different putative genetic lineages. An investigation of the dynamics of co-infections revealed a synergistic effect between CoV and IAV, whereby Coy prevalence was higher given that the birds were co-infected with IAV. There were no interactive effects between IAV and APMV-1. Disease dynamics are the result of an interplay between parasites, host immune responses, and resources; and is imperative that we begin to include all factors to better understand infectious disease risk. (C) 2014 Elsevier B.V. All rights reserved.

Keyword
Avian paramyxovirus, Co-infection, Coronavirus, Disease dynamics, Influenza A virus, Newcastle disease virus
National Category
Microbiology
Research subject
Natural Science, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-40410 (URN)10.1016/j.meegid.2014.11.014 (DOI)000348087400018 ()25461850 (PubMedID)2-s2.0-84912122876 (Scopus ID)
Available from: 2015-02-25 Created: 2015-02-25 Last updated: 2017-12-04Bibliographically approved
5. Infected or not: are PCR-positive oropharyngeal swabs indicative of low pathogenic influenza A virus infection in the respiratory tract of Mallard Anas platyrhynchos?
Open this publication in new window or tab >>Infected or not: are PCR-positive oropharyngeal swabs indicative of low pathogenic influenza A virus infection in the respiratory tract of Mallard Anas platyrhynchos?
2014 (English)In: Veterinary research (Print), ISSN 0928-4249, E-ISSN 1297-9716, Vol. 45, p. Article ID: 53-Article in journal (Refereed) Published
Abstract [en]

Detection of influenza virus in oropharyngeal swabs collected during wild bird surveillance is assumed to representrespiratory infection, although intestine is the main site of infection. We tested this assumption by histologicalexamination of the respiratory tract of wild Mallards with virus-positive oropharyngeal swabs. Thirty-two of 125Mallards tested had viral-RNA positive oropharyngeal swabs. The respiratory tracts of four Mallards with the mostvirus were examined in detail by immunohistochemistry. None had detectable virus antigen in the respiratory tract,suggesting it was not infected. An alternative explanation is that the oropharynx was contaminated with virusthrough feeding in surface water or through preening.

National Category
Microbiology
Research subject
Natural Science, Zoonotic Ecology
Identifiers
urn:nbn:se:lnu:diva-34673 (URN)10.1186/1297-9716-45-53 (DOI)000336928100001 ()2-s2.0-84902380893 (Scopus ID)
Available from: 2014-06-04 Created: 2014-06-04 Last updated: 2017-12-05Bibliographically approved

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