Influenza A virus evolution and spatio-temporal dynamics in Eurasian wild birds: a phylogenetic and phylogeographical study of whole-genome sequence data

Lewis, Nicola S.; Verhagen, Josanne H.; Javakhishvili, Z.; Russell, Colin A.; Lexmond, Pascal; Westgeest, Kim B.; Bestebroer, Theo M.; Halpin, Rebecca; Lin, Xudong; Ransier, Amy; Fedorova, Nadia; Stockwell, Timothy B.; Latorre‐Margalef, Neus; Olsén, Björn; Smith, Gavin J. D.; Bahl, Justin; Wentworth, David E.; Waldenström, Jonas; Fouchier, Ron A. M.; Graaf, Miranda de

doi:10.1099/vir.0.000155

Cited by 23 publications

(20 citation statements)

References 43 publications

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“…The coalescent model with constant population was used as tree model, with a relaxed lognormal clock model. For the mean rate, a prior of 0.002 was used (57). For all data sets, the Monte Carlo Markov chain (MCMC) was run in triplicate for 50 to 100 million generations.…”

Section: Methodsmentioning

confidence: 99%

Evidence of Intercontinental Spread and Uncommon Variants of Low-Pathogenicity Avian Influenza Viruses in Ducks Overwintering in Guatemala

Gonzalez‐Reiche

Nelson

Angel

et al. 2017

mSphere

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Recent outbreaks of highly pathogenic H7N3, H5Nx, and H7N8 avian influenza viruses in North America were introduced by migratory birds, underscoring the importance of understanding how wild birds contribute to the dissemination and evolution of IAVs in nature. At least four of the main IAV duck host species in North America migrate through or overwinter within a narrow strip of Central America, providing opportunities for diverse IAV lineages to mix and exchange gene segments. By obtaining whole-genome sequences of 68 IAV isolates collected from migratory waterfowl in Guatemala (2010 to 2013), the largest data set available from Central America to date, we detected extensive viral diversity, including gene variants rarely found in North America and gene segments of Eurasian origin. Our findings highlight the need for increased IAV surveillance across the geographical span of bird migration flyways, including Neotropical regions that have been vastly undersampled to date.

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Section: Methodsmentioning

confidence: 99%

Evidence of Intercontinental Spread and Uncommon Variants of Low-Pathogenicity Avian Influenza Viruses in Ducks Overwintering in Guatemala

Gonzalez‐Reiche

Nelson

Angel

et al. 2017

mSphere

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“…This natural phenomenon offers a powerful mechanism for AIVs to spread over long distances, connecting spatially disjunct localities and creating opportunities for viral transmission to those wild bird species and poultry resident in disparate geographic localities (7). Indeed, migrating wild birds have been linked to the geographic diffusion of a variety of types of AIV (3), including highly pathogenic H5N1 influenza virus (8)(9)(10)(11), as well as other RNA viruses such as West Nile virus (12,13).…”

Section: Significance Statementmentioning

confidence: 99%

The Impact of Migratory Flyways on the Spread of Avian Influenza Virus in North America

Fourment

Darling

Holmes

2016

Preprint

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Background: Wild birds are the major reservoir hosts for influenza A viruses (AIVs) and have been implicated in the emergence of pandemic events in livestock and human populations. Understanding how AIVs spread within and across continents is therefore critical to the development of successful strategies to manage and reduce the impact of influenza outbreaks. In North America many bird species undergo seasonal migratory movements along a North-South axis, thereby providing opportunities for viruses to spread over long distances. However, the role played by such avian flyways in shaping the genetic structure of AIV populations remains uncertain. Results: To assess the relative contribution of bird migration along flyways to the genetic structure of AIV we performed a large-scale phylogeographic study of viruses sampled in the USA and Canada, involving the analysis of 3805 to 4505 sequences from 36 to 38 geographic localities depending on the gene segment data set. To assist in this we developed a maximum likelihood-based genetic algorithm to explore a wide range of complex spatial models, depicting a more complete picture of the migration network than determined previously. Conclusions: Based on phylogenies estimated from nucleotide sequence data sets, our results show that AIV migration rates are significantly higher within than between flyways, indicating that the migratory patterns of birds play a key role in viral dispersal. These findings provide valuable insights into the evolution, maintenance and transmission of AIVs, in turn allowing the development of improved programs for surveillance and risk assessment.

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“…Reassortment between human H1N1 and H3N2 lineages is detected more rarely but gave rise to an H1N2 virus that circulated widely in the United Kingdom in 2001-2002 (20, 21). Reassortment among avian influenza viruses in birds is highly prevalent and has a major impact on viral population structure in avian reservoirs (22)(23)(24)(25)(26)(27)(28)(29)(30). Thus, reassortment between IAV from two distinct sources occurs in nature and can have major consequences for the epidemiology of the virus in humans and other natural hosts.…”

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confidence: 99%

Influenza A Virus Coinfection through Transmission Can Support High Levels of Reassortment

Tao

White

et al. 2015

J Virol

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The reassortment of gene segments between influenza viruses increases genomic diversity and plays an important role in viral evolution. We have shown previously that this process is highly efficient within a coinfected cell and, given synchronous coinfection at moderate or high doses, can give rise to ϳ60 to 70% of progeny shed from an animal host. Conversely, reassortment in vivo can be rendered undetectable by lowering viral doses or extending the time between infections. One might also predict that seeding of transmitted viruses into different sites within the target tissue could limit subsequent reassortment. Given the potential for stochastic factors to restrict reassortment during natural infection, we sought to determine its efficiency in a host coinfected through transmission. Two scenarios were tested in a guinea pig model, using influenza A/Panama/2007/99 (H3N2) virus (wt) and a silently mutated variant (var) thereof as parental virus strains. In the first, coinfection was achieved by exposing a naive guinea pig to two cagemates, one infected with wt and the other with var virus. When such exposure led to coinfection, robust reassortment was typically seen, with 50 to 100% of isolates carrying reassortant genomes at one or more time points. In the second scenario, naive guinea pigs were exposed to a cagemate that had been coinoculated with wt and var viruses. Here, reassortment occurred in the coinoculated donor host, multiple variants were transmitted, and reassortants were prevalent in the recipient host. Together, these results demonstrate the immense potential for reassortment to generate viral diversity in nature. IMPORTANCE Influenza viruses evolve rapidly under selection due to the generation of viral diversity through two mechanisms. The first is the introduction of random errors into the genome by the viral polymerase, which occurs with a frequency of approximately 10؊5 errors/nucleotide replicated. The second is reassortment, or the exchange of gene segments between viruses. Reassortment is known to occur readily under well-controlled laboratory conditions, but its frequency in nature is not clear. Here, we tested the hypothesis that reassortment efficiency following coinfection through transmission would be reduced compared to that seen with coinoculation. Contrary to this hypothesis, our results indicate that coinfection achieved through transmission supports high levels of reassortment. These results suggest that reassortment is not exquisitely sensitive to stochastic effects associated with transmission and likely occurs in nature whenever a host is infected productively with more than one influenza A virus.T he segmented nature of the influenza virus genome allows for ready exchange of genetic material between two viruses that coinfect one cell (1). If the parental viruses differ in all eight gene segments, 256 different progeny viruses can be produced in a single reassortment event. Reassortment between two very distinct strains is typically associated with marked genotypic and ...

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Influenza A virus evolution and spatio-temporal dynamics in Eurasian wild birds: a phylogenetic and phylogeographical study of whole-genome sequence data

Cited by 23 publications

References 43 publications

Evidence of Intercontinental Spread and Uncommon Variants of Low-Pathogenicity Avian Influenza Viruses in Ducks Overwintering in Guatemala

Evidence of Intercontinental Spread and Uncommon Variants of Low-Pathogenicity Avian Influenza Viruses in Ducks Overwintering in Guatemala

The Impact of Migratory Flyways on the Spread of Avian Influenza Virus in North America

Influenza A Virus Coinfection through Transmission Can Support High Levels of Reassortment

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