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Genetic structure of Pacific Flyway avian influenza viruses is shaped by geographic location, host species, and sampling period

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Abstract

The eight gene segments of avian influenza virus (AIV) reassort frequently and rapidly to generate novel genotypes and subtypes that are transmissible to a broad range of hosts. There is evidence that AIV can have a restricted host range and can segregate in space and time. Host–virus relationships at the species, geographic, and spatial scales have not been fully defined for AIV populations of the Pacific Flyway, particularly among the diverse waterfowl that occupy the Flyway in Alaska and California. Using the sequence analysis program Bayesian Tip-association Significance testing (BaTS) created for analysis of phylogeny–trait associations, we determined whether the genetic structure of Pacific Flyway AIVs sampled between 2006 and 2008 was influenced by the host species, geographic location of virus collection, and time of sampling. In posterior sets of trees, genetically similar viruses clustered by host species for thick-billed murres and glaucous gulls (order Charadriiformes), and for northern shovelers, northern pintails, and mallards (order Anseriformes). AIVs from Alaska and California were strongly spatially structured, clustering separately by region across all segments. The timing of sampling influenced the genetic structure of California AIV gene segments, possibly reflecting waves of host species movement into wintering areas. The strength of phylogeny–trait association varied by virus segment and by trait of interest, which we hypothesize is related to the frequent genetic reassortment and interspecies transmission in waterfowl.

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References

  1. K.K. VanDalen, A.B. Franklin, N.L. Mooers, H.J. Sullivan, S.A. Shriner, PLoS ONE 5, e12851 (2010)

    Article  PubMed  Google Scholar 

  2. R.G. Webster, W.J. Bean, O.T. Gorman, T.M. Chambers, Y. Kawaoka, Microbiol. Rev. 56, 152–179 (1992)

    PubMed  CAS  Google Scholar 

  3. J.D. Brown, G. Goekjian, R. Poulson, S. Valeika, D.E. Stallknecht, Vet. Microbiol. 136, 20–26 (2009)

    Article  PubMed  Google Scholar 

  4. C.A. Macken, R.J. Webby, W.J. Bruno, J. Gen. Virol. 87, 2803–2815 (2006)

    Article  PubMed  CAS  Google Scholar 

  5. V.G. Dugan, R. Chen, D.J. Spiro, N. Sengamalay, J. Zaborsky, E. Ghedin, J. Nolting, D.E. Swayne, J.A. Runstadler, G.M. Happ, D.A. Senne, R. Wang, R.D. Slemons, E.C. Holmes, J.K. Taubenberger, PLoS Pathog. 4, e1000076 (2008)

    Article  PubMed  Google Scholar 

  6. R. Chen, E.C. Holmes, Virology 383, 156–161 (2009)

    Article  PubMed  CAS  Google Scholar 

  7. B. Olsen, V.J. Munster, A. Wallensten, J. Waldenstrom, A.D. Osterhaus, R.A. Fouchier, Science 312, 384–388 (2006)

    Article  PubMed  CAS  Google Scholar 

  8. A.M. Ramey, J.M. Pearce, A.B. Reeves, J.C. Franson, M.R. Petersen, H.S. Ip, Arch. Virol. 156, 1813–1821 (2011)

    Article  PubMed  CAS  Google Scholar 

  9. Y. Kawaoka, T.M. Chambers, W.L. Sladen, R.G. Webster, Virology 163, 247–250 (1988)

    Article  PubMed  CAS  Google Scholar 

  10. J.L. Siembieda, C.K. Johnson, C. Cardona, N. Anchell, N. Dao, W. Reisen, W. Boyce, Vector Borne Zoonotic Dis. 10, 793–800 (2010)

    Article  PubMed  Google Scholar 

  11. S. Krauss, D. Walker, S.P. Pryor, L. Niles, L. Chenghong, V.S. Hinshaw, R.G. Webster, Vector Borne Zoonotic Dis. 4, 177–189 (2004)

    Article  PubMed  Google Scholar 

  12. V.J. Munster, C. Baas, P. Lexmond, J. Waldenstrom, A. Wallensten, T. Fransson, G.F. Rimmelzwaan, W.E. Beyer, M. Schutten, B. Olsen, A.D. Osterhaus, R.A. Fouchier, PLoS Pathog. 3, e61 (2007)

    Article  PubMed  Google Scholar 

  13. R.A. Fouchier, V. Munster, A. Wallensten, T.M. Bestebroer, S. Herfst, D. Smith, G.F. Rimmelzwaan, B. Olsen, A.D. Osterhaus, J. Virol. 79, 2814–2822 (2005)

    Article  PubMed  CAS  Google Scholar 

  14. E. Jourdain, D. van Riel, V.J. Munster, T. Kuiken, J. Waldenstrom, B. Olsen, P. Ellstrom, PLoS ONE 6, e24155 (2011)

    Article  PubMed  CAS  Google Scholar 

  15. M. Matrosovich, J. Stech, H.D. Klenk, Rev. Sci. Tech. 28, 203–217 (2009)

    PubMed  CAS  Google Scholar 

  16. V.J. Munster, R.A. Fouchier, Vaccine 27, 6340–6344 (2009)

    Article  PubMed  CAS  Google Scholar 

  17. G.C. Boere, D.A. Stroud, in Waterbirds Around the World, ed. by G.C. Boere, C.A. Galbraith, D.A. Stroud (The Stationary Office, Edinburgh, 2006), p. 8

    Google Scholar 

  18. P.L. Flint, K. Ozaki, J.M. Pearce, B. Guzzetti, H. Higuchi, J.P. Fleskes, T. Shimada, D.V. Derksen, Condor 111, 8 (2009)

    Article  Google Scholar 

  19. K. Sugiura, M. Yamamoto, T. Nishida, D. Tsukamoto, T. Saito, T. Onodera, Rev. Sci. Tech. 28, 1005–1013 (2009)

    PubMed  CAS  Google Scholar 

  20. World Health Organization, H5N1 avian influenza: timeline of major events, November 7, 2011. http://www.who.int/influenza/human_animal_interface/en/. Accessed November 2011

  21. A.M. Ramey, J.M. Pearce, C.R. Ely, L.M. Guy, D.B. Irons, D.V. Derksen, H.S. Ip, Virology 406, 352–359 (2010)

    Article  PubMed  CAS  Google Scholar 

  22. T. Nakano, L. Lu, P. Liu, O.G. Pybus, J. Infect. Dis. 190, 1098–1108 (2004)

    Article  PubMed  CAS  Google Scholar 

  23. J. Parker, A. Rambaut, O.G. Pybus, Infect. Genet. Evol. 8, 239–246 (2008)

    Article  PubMed  CAS  Google Scholar 

  24. K. Katoh, K. Misawa, K. Kuma, T. Miyata, Nucleic Acids Res. 30, 3059–3066 (2002)

    Article  PubMed  CAS  Google Scholar 

  25. A.J. Drummond, B. Ashton, M. Cheung, J. Heled, M. Kearse, R. Moir, S. Stones-Havas, T. Thierer, A. Wilson, Geneious v.4.7., 2009

  26. A.M. Ramey, J.M. Pearce, P.L. Flint, H.S. Ip, D.V. Derksen, J.C. Franson, M.J. Petrula, B.D. Scotton, K.M. Sowl, M.L. Wege, K.A. Trust, Virology 401, 179–189 (2010)

    Article  PubMed  CAS  Google Scholar 

  27. A.V. Koehler, J.M. Pearce, P.L. Flint, J.C. Franson, H.S. Ip, Mol. Ecol. 17, 4754–4762 (2008)

    Article  PubMed  Google Scholar 

  28. J.M. Pearce, A.M. Ramey, H.S. Ip, R.E. Gill Jr., Virus Res. 148, 44–50 (2010)

    Article  PubMed  CAS  Google Scholar 

  29. J.A. Nylander, MrModeltest v2, Program distributed by author (Evolutionary Biology Centre, Uppsala University, Uppsala, 2004)

    Google Scholar 

  30. J.P. Huelsenbeck, F. Ronquist, Bioinformatics 17, 754–755 (2001)

    Article  PubMed  CAS  Google Scholar 

  31. F. Ronquist, J.P. Huelsenbeck, Bioinformatics 19, 1572–1574 (2003)

    Article  PubMed  CAS  Google Scholar 

  32. J.A. Nylander, J.C. Wilgenbush, D.L. Warren, D.L. Swofford, Bioinformatics 24, 3 (2008)

    Article  Google Scholar 

  33. T.H. Wang, Y.K. Donaldson, R.P. Brettle, J.E. Bell, P. Simmonds, J. Virol. 75, 11686–11699 (2001)

    Article  PubMed  CAS  Google Scholar 

  34. M. Slatkin, W.P. Maddison, Genetics 123, 603–613 (1989)

    PubMed  CAS  Google Scholar 

  35. W.M. Fitch, Syst. Zool. 20, 11 (1971)

    Article  Google Scholar 

  36. H.S. Ip, P.L. Flint, J.C. Franson, R.J. Dusek, D.V. Derksen, R.E. Gill Jr., C.R. Ely, J.M. Pearce, R.B. Lanctot, S.M. Matsuoka, D.B. Irons, J.B. Fischer, R.M. Oates, M.R. Petersen, T.F. Fondell, D.A. Rocque, J.C. Pedersen, T.C. Rothe, Virol. J. 5, 71 (2008). doi:10.1186/1743-422X-5-71

    Article  PubMed  Google Scholar 

  37. N.J. Hill, J.Y. Takekawa, C.M. Cardona, B.W. Meixell, J.A. Runstadler, W.M. Boyce, Vector Borne Zoonotic Dis. (2011). doi:10.1089/vbz.2010.0246

  38. J.M. Pearce, A.M. Ramey, P.L. Flint, A.V. Koehler, J.P. Fleskes, J.C. Franson, J.S. Hall, D.V. Derksen, H.S. Ip, Evol. Appl. 2, 12 (2009)

    Article  Google Scholar 

  39. S. Krauss, C.A. Obert, J. Franks, D. Walker, K. Jones, P. Seiler, L. Niles, S.P. Pryor, J.C. Obenauer, C.W. Naeve, L. Widjaja, R.J. Webby, R.G. Webster, PLoS Pathog. 3, e167 (2007)

    Article  PubMed  Google Scholar 

  40. T.T. Lam, H.S. Ip, E. Ghedin, D.E. Wentworth, R.A. Halpin, T.B. Stockwell, D.J. Spiro, R.J. Dusek, J.B. Bortner, J. Hoskins, B.D. Bales, D.R. Yparraguirre, E.C. Holmes, Ecol. Lett. (2011). doi:10.1111/j.1461-0248.2011.01703.x

  41. M.R. Miller, J.Y. Takekawa, J.P. Fleskes, D.L. Orthmeyer, M.L. Cassaza, W.M. Perry, Can. J. Zool. 83, 19 (2005)

    Article  Google Scholar 

  42. C.A. Nicolai, P.L. Flint, M. Wege, J. Wildl. Manag. 69, 9 (2005)

    Google Scholar 

  43. F.C. Bellrose, Ducks, Geese and Swans of North America (Stackpole Books, Harrisburg, 1980)

    Google Scholar 

  44. J. Bahl, D. Vijaykrishna, E.C. Holmes, G.J. Smith, Y. Guan, Virology 390, 289–297 (2009)

    Article  PubMed  CAS  Google Scholar 

  45. R. Chen, E.C. Holmes, J. Mol. Evol. 70, 98–105 (2010)

    Article  PubMed  CAS  Google Scholar 

  46. M. ElHefnawi, O. Alaidi, N. Mohamed, M. Kamar, I. El-Azab, S. Zada, R. Siam, Virol. J. 8, 44 (2011). doi:10.1186/1743-422X-8-44

    PubMed  CAS  Google Scholar 

  47. N.J. Hill, J.Y. Takekawa, C.J. Cardona, J.T. Ackerman, A.K. Schultz, K.A. Spragens, W.M. Boyce, Avian Dis. 54, 426–432 (2010)

    Article  PubMed  Google Scholar 

  48. V.S. Hinshaw, G.M. Air, A.J. Gibbs, L. Graves, B. Prescott, D. Karunakaran, J. Virol. 42, 865–872 (1982)

    PubMed  CAS  Google Scholar 

  49. D. Kleijn, V.J. Munster, B.S. Ebbinge, D.A. Jonkers, G.J. Muskens, Y. Van Randen, R.A. Fouchier, Proc. Biol. Sci. 277, 2041–2048 (2010)

    Article  PubMed  CAS  Google Scholar 

  50. Cornell Laboratory of Ornithology, Birds of North America Online. http://bna.birds.cornell.edu/bna/. Accessed November 2011

  51. B.J. Hoye, V.J. Munster, H. Nishiura, M. Klaassen, R.A. Fouchier, Emerg. Infect. Dis. 16, 1827–1834 (2010)

    PubMed  Google Scholar 

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Acknowledgments

We thank the field and laboratory personnel at the University of Alaska Fairbanks and the University of California Davis who were involved in bird sampling and processing of virus isolates for analysis. Thanks to Tracey Goldstein (UC Davis) and Tasha Belfiore for helpful guidance on the data analysis and manuscript preparation. Funding for this research was provided by the National Institute of Allergy and Infectious Disease (contract HHSN266200700009C).

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Correspondence to Yvette A. Girard.

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Girard, Y.A., Runstadler, J.A., Aldehoff, F. et al. Genetic structure of Pacific Flyway avian influenza viruses is shaped by geographic location, host species, and sampling period. Virus Genes 44, 415–428 (2012). https://doi.org/10.1007/s11262-011-0706-5

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