Evolution and Ecology of Influenza A Viruses

  • Sun-Woo Yoon
  • Richard J. Webby
  • Robert G. WebsterEmail author
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 385)


Wild aquatic bird populations have long been considered the natural reservoir for influenza A viruses with virus transmission from these birds seeding other avian and mammalian hosts. While most evidence still supports this dogma, recent studies in bats have suggested other reservoir species may also exist. Extensive surveillance studies coupled with an enhanced awareness in response to H5N1 and pandemic 2009 H1N1 outbreaks is also revealing a growing list of animals susceptible to infection with influenza A viruses. Although in a relatively stable host–pathogen interaction in aquatic birds, antigenic, and genetic evolution of influenza A viruses often accompanies interspecies transmission as the virus adapts to a new host. The evolutionary changes in the new hosts result from a number of processes including mutation, reassortment, and recombination. Depending on host and virus these changes can be accompanied by disease outbreaks impacting wildlife, veterinary, and public health.


Influenza Virus Wild Bird Harbor Seal Swine Influenza Virus Highly Pathogenic 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This work was supported by Contract No. HHSN266200700005C from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, and by ALSAC. We thank James Knowles for manuscript preparation.


  1. Anthony SJ, St Leger JA, Pugliares K, Ip HS, Chan JM, Carpenter ZW, Navarrete-Macias I, Sanchez-Leon M, Saliki JT, Pedersen J, Karesh W, Daszak P, Rabadan R, Rowles T, Lipkin WI (2012) Emergence of fatal avian influenza in New England harbor seals. MBio 3:e00166-12Google Scholar
  2. Bahl J, Nelson MI, Chan KH, Chen R, Vijaykrishna D, Halpin RA, Stockwell TB, Lin X, Wentworth DE, Ghedin E, Guan Y, Peiris JS, Riley S, Rambaut A, Holmes EC, Smith GJ (2011) Temporally structured metapopulation dynamics and persistence of influenza A H3N2 virus in humans. Proc Natl Acad Sci USA 108:19359–19364PubMedCrossRefPubMedCentralGoogle Scholar
  3. Becker WB (1966) The isolation and classification of Tern virus: influenza A-Tern South Africa—1961. J Hyg (Lond) 64:309–320CrossRefGoogle Scholar
  4. Bryant NA, Paillot R, Rash AS, Medcalf E, Montesso F, Ross J, Watson J, Jeggo M, Lewis NS, Newton JR, Elton DM (2010) Comparison of two modern vaccines and previous influenza infection against challenge with an equine influenza virus from the Australian 2007 outbreak. Vet Res 41:19PubMedCrossRefPubMedCentralGoogle Scholar
  5. Buonavoglia C, Martella V (2007) Canine respiratory viruses. Vet Res 38:355–373PubMedCrossRefGoogle Scholar
  6. Callan RJ, Early G, Kida H, Hinshaw VS (1995) The appearance of H3 influenza viruses in seals. J Gen Virol 76(Pt 1):199–203PubMedCrossRefGoogle Scholar
  7. Castleman WL, Powe JR, Crawford PC, Gibbs EP, Dubovi EJ, Donis RO, Hanshaw D (2010) Canine H3N8 influenza virus infection in dogs and mice. Vet Pathol 47:507–517PubMedCrossRefGoogle Scholar
  8. Crawford PC, Dubovi EJ, Castleman WL, Stephenson I, Gibbs EP, Chen L, Smith C, Hill RC, Ferro P, Pompey J, Bright RA, Medina MJ, Johnson CM, Olsen CW, Cox NJ, Klimov AI, Katz JM, Donis RO (2005) Transmission of equine influenza virus to dogs. Science 310:482–485PubMedCrossRefGoogle Scholar
  9. Daly JM, Lai AC, Binns MM, Chambers TM, Barrandeguy M, Mumford JA (1996) Antigenic and genetic evolution of equine H3N8 influenza A viruses. J Gen Virol 77(Pt 4):661–671PubMedCrossRefGoogle Scholar
  10. de Jong JC, Smith DJ, Lapedes AS, Donatelli I, Campitelli L, Barigazzi G, Van Reeth K, Jones TC, Rimmelzwaan GF, Osterhaus AD, Fouchier RA (2007) Antigenic and genetic evolution of swine influenza A (H3N2) viruses in Europe. J Virol 81:4315–4322PubMedCrossRefPubMedCentralGoogle Scholar
  11. Ducatez MF, Hause B, Stigger-Rosser E, Darnell D, Corzo C, Juleen K, Simonson R, Brockwell-Staats C, Rubrum A, Wang D, Webb A, Crumpton JC, Lowe J, Gramer M, Webby RJ (2011) Multiple reassortment between pandemic (H1N1) 2009 and endemic influenza viruses in pigs, United States. Emerg Infect Dis 17:1624–1629PubMedCrossRefPubMedCentralGoogle Scholar
  12. Dundon WG, De Benedictis P, Viale E, Capua I (2010) Serologic evidence of pandemic (H1N1) 2009 infection in dogs, Italy. Emerg Infect Dis 16:2019–2021PubMedCrossRefPubMedCentralGoogle Scholar
  13. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, Chin CR, Feeley EM, Sims JS, Adams DJ, Wise HM, Kane L, Goulding D, Digard P, Anttila V, Baillie JK, Walsh TS, Hume DA, Palotie A, Xue Y, Colonna V, Tyler-Smith C, Dunning J, Gordon SB, Gen II, Investigators M, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P (2012) IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519–523PubMedCrossRefPubMedCentralGoogle Scholar
  14. Fouchier RA, Guan Y (2013) Ecology and evolution of influenza viruses in wild and domestic birds, 2nd edn. Wiley, London Google Scholar
  15. Fouchier RA, Munster V, Wallensten A, Bestebroer TM, Herfst S, Smith D, Rimmelzwaan GF, Olsen B, Osterhaus AD (2005) Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J Virol 79:2814–2822PubMedCrossRefPubMedCentralGoogle Scholar
  16. Garten RJ, Davis CT, Russell CA, Shu B, Lindstrom S, Balish A, Sessions WM, Xu X, Skepner E, Deyde V, Okomo-Adhiambo M, Gubareva L, Barnes J, Smith CB, Emery SL, Hillman MJ, Rivailler P, Smagala J, de Graaf M, Burke DF, Fouchier RA, Pappas C, Alpuche-Aranda CM, Lopez-Gatell H, Olivera H, Lopez I, Myers CA, Faix D, Blair PJ, Yu C, Keene KM, Dotson PD Jr, Boxrud D, Sambol AR, Abid SH, St George K, Bannerman T, Moore AL, Stringer DJ, Blevins P, Demmler-Harrison GJ, Ginsberg M, Kriner P, Waterman S, Smole S, Guevara HF, Belongia EA, Clark PA, Beatrice ST, Donis R, Katz J, Finelli L, Bridges CB, Shaw M, Jernigan DB, Uyeki TM, Smith DJ, Klimov AI, Cox NJ (2009) Antigenic and genetic characteristics of swine-origin 2009 A(H1N1) influenza viruses circulating in humans. Science 325:197–201Google Scholar
  17. Geraci JR, St Aubin DJ, Barker IK, Webster RG, Hinshaw VS, Bean WJ, Ruhnke HL, Prescott JH, Early G, Baker AS, Madoff S, Schooley RT (1982) Mass mortality of harbor seals: pneumonia associated with influenza A virus. Science 215:1129–1131Google Scholar
  18. Giese M, Harder TC, Teifke JP, Klopfleisch R, Breithaupt A, Mettenleiter TC, Vahlenkamp TW (2008) Experimental infection and natural contact exposure of dogs with avian influenza virus (H5N1). Emerg Infect Dis 14:308–310PubMedCrossRefPubMedCentralGoogle Scholar
  19. Gog JR, Rimmelzwaan GF, Osterhaus AD, Grenfell BT (2003) Population dynamics of rapid fixation in cytotoxic T lymphocyte escape mutants of influenza A. Proc Natl Acad Sci USA 100:11143–11147PubMedCrossRefPubMedCentralGoogle Scholar
  20. Goldstein T, Mena I, Anthony SJ, Medina R, Robinson PW, Greig DJ, Costa DP, Lipkin WI, Garcia-Sastre A, Boyce WM (2013) Pandemic H1N1 influenza isolated from free-ranging Northern Elephant Seals in 2010 off the central California coast. PLoS One 8:e62259PubMedCrossRefPubMedCentralGoogle Scholar
  21. Guan Y, Shortridge KF, Krauss S, Webster RG (1999) Molecular characterization of H9N2 influenza viruses: were they the donors of the “internal” genes of H5N1 viruses in Hong Kong? Proc Natl Acad Sci USA 96:9363–9367PubMedCrossRefPubMedCentralGoogle Scholar
  22. Guo Y, Wang M, Kawaoka Y, Gorman O, Ito T, Saito T, Webster RG (1992) Characterization of a new avian-like influenza A virus from horses in China. Virology 188:245–255PubMedCrossRefGoogle Scholar
  23. Guo Y, Wang M, Zheng GS, Li WK, Kawaoka Y, Webster RG (1995) Seroepidemiological and molecular evidence for the presence of two H3N8 equine influenza viruses in China in 1993–94. J Gen Virol 76(Pt 8):2009–2014PubMedCrossRefGoogle Scholar
  24. Hansbro PM, Warner S, Tracey JP, Arzey KE, Selleck P, O’Riley K, Beckett EL, Bunn C, Kirkland PD, Vijaykrishna D, Olsen B, Hurt AC (2010) Surveillance and analysis of avian influenza viruses, Australia. Emerg Infect Dis 16:1896–1904PubMedCrossRefPubMedCentralGoogle Scholar
  25. Hinshaw VS, Bean WJ, Geraci J, Fiorelli P, Early G, Webster RG (1986) Characterization of two influenza A viruses from a pilot whale. J Virol 58:655–656PubMedPubMedCentralGoogle Scholar
  26. Hinshaw VS, Webster RG, Easterday BC, Bean WJ Jr (1981) Replication of avian influenza A viruses in mammals. Infect Immun 34:354–361PubMedPubMedCentralGoogle Scholar
  27. Horby P, Nguyen NY, Dunstan SJ, Baillie JK (2013) An updated systematic review of the role of host genetics in susceptibility to influenza. Influenza Other Respir Viruses 7(Suppl 2):37–41PubMedCrossRefGoogle Scholar
  28. Howard WA, Essen SC, Strugnell BW, Russell C, Barass L, Reid SM, Brown IH (2011) Reassortant Pandemic (H1N1) 2009 virus in pigs, United Kingdom. Emerg Infect Dis 17:1049–1052PubMedCrossRefPubMedCentralGoogle Scholar
  29. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, Castrucci MR, Donatelli I, Kida H, Paulson JC, Webster RG, Kawaoka Y (1998) Molecular basis for the generation in pigs of influenza A viruses with pandemic potential. J Virol 72:7367–7373PubMedPubMedCentralGoogle Scholar
  30. Kay RM, Done SH, Paton DJ (1994) Effect of sequential porcine reproductive and respiratory syndrome and swine influenza on the growth and performance of finishing pigs. Vet Rec 135:199–204PubMedCrossRefGoogle Scholar
  31. Krauss S, Walker D, Pryor SP, Niles L, Chenghong L, Hinshaw VS, Webster RG (2004) Influenza A viruses of migrating wild aquatic birds in North America. Vector Borne Zoonotic Dis 4:177–189PubMedCrossRefGoogle Scholar
  32. Kuiken T, Rimmelzwaan G, van Riel D, van Amerongen G, Baars M, Fouchier R, Osterhaus A (2004) Avian H5N1 influenza in cats. Science 306:241PubMedCrossRefGoogle Scholar
  33. Latorre-Margalef N, Gunnarsson G, Munster VJ, Fouchier RA, Osterhaus AD, Elmberg J, Olsen B, Wallensten A, Haemig PD, Fransson T, Brudin L, Waldenstrom J (2009) Effects of influenza A virus infection on migrating mallard ducks. Proc Biol Sci 276:1029–1036PubMedCrossRefPubMedCentralGoogle Scholar
  34. Lee C, Song D, Kang B, Kang D, Yoo J, Jung K, Na G, Lee K, Park B, Oh J (2009) A serological survey of avian origin canine H3N2 influenza virus in dogs in Korea. Vet Microbiol 137:359–362PubMedCrossRefGoogle Scholar
  35. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, Russell CA, Smith DJ, Pybus OG, Brockmann D, Suchard MA (2014) Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog 10:e1003932PubMedCrossRefPubMedCentralGoogle Scholar
  36. Li S, Shi Z, Jiao P, Zhang G, Zhong Z, Tian W, Long LP, Cai Z, Zhu X, Liao M, Wan XF (2010) Avian-origin H3N2 canine influenza A viruses in Southern China. Infect Genet Evol 10:1286–1288PubMedCrossRefPubMedCentralGoogle Scholar
  37. Lindstrom S, Garten R, Balish A, Shu B, Emery S, Berman L, Barnes N, Sleeman K, Gubareva L, Villanueva J, Klimov A (2012) Human infections with novel reassortant influenza A(H3N2)v viruses, United States, 2011. Emerg Infect Dis 18:834–837PubMedCrossRefPubMedCentralGoogle Scholar
  38. Lorusso A, Vincent AL, Harland ML, Alt D, Bayles DO, Swenson SL, Gramer MR, Russell CA, Smith DJ, Lager KM, Lewis NS (2011) Genetic and antigenic characterization of H1 influenza viruses from United States swine from 2008. J Gen Virol 92:919–930PubMedCrossRefPubMedCentralGoogle Scholar
  39. Maas R, Tacken M, Ruuls L, Koch G, van Rooij E, Stockhofe-Zurwieden N (2007) Avian influenza (H5N1) susceptibility and receptors in dogs. Emerg Infect Dis 13:1219–1221PubMedCrossRefPubMedCentralGoogle Scholar
  40. McCullers JA, Van De Velde LA, Schultz RD, Mitchell CG, Halford CR, Boyd KL, Schultz-Cherry S (2011) Seroprevalence of seasonal and pandemic influenza A viruses in domestic cats. Arch Virol 156:117–120PubMedCrossRefGoogle Scholar
  41. Moreno A, Di Trani L, Faccini S, Vaccari G, Nigrelli D, Boniotti MB, Falcone E, Boni A, Chiapponi C, Sozzi E, Cordioli P (2011) Novel H1N2 swine influenza reassortant strain in pigs derived from the pandemic H1N1/2009 virus. Vet Microbiol 149:472–477PubMedCrossRefGoogle Scholar
  42. Munster VJ, Baas C, Lexmond P, Waldenstrom J, Wallensten A, Fransson T, Rimmelzwaan GF, Beyer WE, Schutten M, Olsen B, Osterhaus AD, Fouchier RA (2007) Spatial, temporal, and species variation in prevalence of influenza A viruses in wild migratory birds. PLoS Pathog 3:e61PubMedCrossRefPubMedCentralGoogle Scholar
  43. Myers KP, Olsen CW, Gray GC (2007) Cases of swine influenza in humans: a review of the literature. Clin Infect Dis 44:1084–1088PubMedCrossRefPubMedCentralGoogle Scholar
  44. Nelson MI, Edelman L, Spiro DJ, Boyne AR, Bera J, Halpin R, Sengamalay N, Ghedin E, Miller MA, Simonsen L, Viboud C, Holmes EC (2008) Molecular epidemiology of A/H3N2 and A/H1N1 influenza virus during a single epidemic season in the United States. PLoS Pathog 4:e1000133PubMedCrossRefPubMedCentralGoogle Scholar
  45. Nelson MI, Gramer MR, Vincent AL, Holmes EC (2012) Global transmission of influenza viruses from humans to swine. J Gen Virol 93:2195–2203PubMedCrossRefPubMedCentralGoogle Scholar
  46. Nfon CK, Berhane Y, Hisanaga T, Zhang S, Handel K, Kehler H, Labrecque O, Lewis NS, Vincent AL, Copps J, Alexandersen S, Pasick J (2011) Characterization of H1N1 swine influenza viruses circulating in Canadian pigs in 2009. J Virol 85:8667–8679PubMedCrossRefPubMedCentralGoogle Scholar
  47. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA (2006) Global patterns of influenza A virus in wild birds. Science 312:384–388PubMedCrossRefGoogle Scholar
  48. Olsen CW, Karasin A, Erickson G (2003) Characterization of a swine-like reassortant H1N2 influenza virus isolated from a wild duck in the United States. Virus Res 93:115–121PubMedCrossRefGoogle Scholar
  49. Osterhaus AD, Rimmelzwaan GF, Martina BE, Bestebroer TM, Fouchier RA (2000) Influenza B virus in seals. Science 288:1051–1053PubMedCrossRefGoogle Scholar
  50. Paniker CK, Nair CM (1970) Infection with A2 Hong Kong influenza virus in domestic cats. Bull World Health Organ 43:859–862PubMedPubMedCentralGoogle Scholar
  51. Paniker CK, Nair CM (1972) Experimental infection of animals with influenzavirus types A and B. Bull World Health Organ 47:461–463PubMedPubMedCentralGoogle Scholar
  52. Peiris JS, Guan Y, Markwell D, Ghose P, Webster RG, Shortridge KF (2001) Cocirculation of avian H9N2 and contemporary “human” H3N2 influenza A viruses in pigs in southeastern China: potential for genetic reassortment? J Virol 75:9679–9686PubMedCrossRefPubMedCentralGoogle Scholar
  53. Pereda AJ, Uhart M, Perez AA, Zaccagnini ME, La Sala L, Decarre J, Goijman A, Solari L, Suarez R, Craig MI, Vagnozzi A, Rimondi A, Konig G, Terrera MV, Kaloghlian A, Song H, Sorrell EM, Perez DR (2008) Avian influenza virus isolated in wild waterfowl in Argentina: evidence of a potentially unique phylogenetic lineage in South America. Virology 378:363–370PubMedCrossRefPubMedCentralGoogle Scholar
  54. Perez DR, Lim W, Seiler JP, Yi G, Peiris M, Shortridge KF, Webster RG (2003) Role of quail in the interspecies transmission of H9 influenza A viruses: molecular changes on HA that correspond to adaptation from ducks to chickens. J Virol 77:3148–3156PubMedCrossRefPubMedCentralGoogle Scholar
  55. Romvary J, Rozsa J, Farkas E (1975) Infection of dogs and cats with the Hong Kong influenza A (H3N2) virus during an epidemic period in Hungary. Acta Vet Acad Sci Hung 25:255–259PubMedGoogle Scholar
  56. Shortridge KF (1992) Pandemic influenza: A zoonosis? Semin Respir Infect 7:11–25PubMedGoogle Scholar
  57. Song D, Lee C, Kang B, Jung K, Oh T, Kim H, Park B, Oh J (2009) Experimental infection of dogs with avian-origin canine influenza A virus (H3N2). Emerg Infect Dis 15:56–58PubMedCrossRefPubMedCentralGoogle Scholar
  58. Songserm T, Amonsin A, Jam-on R, Sae-Heng N, Meemak N, Pariyothorn N, Payungporn S, Theamboonlers A, Poovorawan Y (2006) Avian influenza H5N1 in naturally infected domestic cat. Emerg Infect Dis 12:681–683PubMedCrossRefPubMedCentralGoogle Scholar
  59. Sovinova O, Tumova B, Pouska F, Nemec J (1958) Isolation of a virus causing respiratory disease in horses. Acta Virol 2:52–61PubMedGoogle Scholar
  60. Sponseller BA, Strait E, Jergens A, Trujillo J, Harmon K, Koster L, Jenkins-Moore M, Killian M, Swenson S, Bender H, Waller K, Miles K, Pearce T, Yoon KJ, Nara P (2010) Influenza A pandemic (H1N1) 2009 virus infection in domestic cat. Emerg Infect Dis 16:534–537PubMedCrossRefPubMedCentralGoogle Scholar
  61. Suarez DL, Senne DA, Banks J, Brown IH, Essen SC, Lee CW, Manvell RJ, Mathieu-Benson C, Moreno V, Pedersen JC, Panigrahy B, Rojas H, Spackman E, Alexander DJ (2004) Recombination resulting in virulence shift in avian influenza outbreak, Chile. Emerg Infect Dis 10:693–699PubMedCrossRefPubMedCentralGoogle Scholar
  62. Thanawongnuwech R, Amonsin A, Tantilertcharoen R, Damrongwatanapokin S, Theamboonlers A, Payungporn S, Nanthapornphiphat K, Ratanamungklanon S, Tunak E, Songserm T, Vivatthanavanich V, Lekdumrongsak T, Kesdangsakonwut S, Tunhikorn S, Poovorawan Y (2005) Probable tiger-to-tiger transmission of avian influenza H5N1. Emerg Infect Dis 11:699–701PubMedCrossRefPubMedCentralGoogle Scholar
  63. Tong S, Zhu X, Li Y, Shi M, Zhang J, Bourgeois M, Yang H, Chen X, Recuenco S, Gomez J, Chen LM, Johnson A, Tao Y, Dreyfus C, Yu W, McBride R, Carney PJ, Gilbert AT, Chang J, Guo Z, Davis CT, Paulson JC, Stevens J, Rupprecht CE, Holmes EC, Wilson IA, Donis RO (2013) New world bats harbor diverse influenza A viruses. PLoS Pathog 9:e1003657PubMedCrossRefPubMedCentralGoogle Scholar
  64. Tu J, Zhou H, Jiang T, Li C, Zhang A, Guo X, Zou W, Chen H, Jin M (2009) Isolation and molecular characterization of equine H3N8 influenza viruses from pigs in China. Arch Virol 154:887–890PubMedCrossRefGoogle Scholar
  65. United States Department of Agriculture ARS (2014) Animal influenza viruses: gap analysis workshop report.
  66. Uyeki TM, Chong YH, Katz JM, Lim W, Ho YY, Wang SS, Tsang TH, Au WW, Chan SC, Rowe T, Hu-Primmer J, Bell JC, Thompson WW, Bridges CB, Cox NJ, Mak KH, Fukuda K (2002) Lack of evidence for human-to-human transmission of avian influenza A (H9N2) viruses in Hong Kong, China 1999. Emerg Infect Dis 8:154–159PubMedCrossRefPubMedCentralGoogle Scholar
  67. van Gils JA, Munster VJ, Radersma R, Liefhebber D, Fouchier RA, Klaassen M (2007) Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus. PLoS One 2:e184PubMedCrossRefPubMedCentralGoogle Scholar
  68. Vijaykrishna D, Poon LL, Zhu HC, Ma SK, Li OT, Cheung CL, Smith GJ, Peiris JS, Guan Y (2010) Reassortment of pandemic H1N1/2009 influenza A virus in swine. Science 328:1529PubMedCrossRefPubMedCentralGoogle Scholar
  69. Vijaykrishna D, Smith GJ, Pybus OG, Zhu H, Bhatt S, Poon LL, Riley S, Bahl J, Ma SK, Cheung CL, Perera RA, Chen H, Shortridge KF, Webby RJ, Webster RG, Guan Y, Peiris JS (2011) Long-term evolution and transmission dynamics of swine influenza A virus. Nature 473:519–522PubMedCrossRefGoogle Scholar
  70. Vincent A, Awada L, Brown I, Chen H, Claes F, Dauphin G, Donis R, Culhane M, Hamilton K, Lewis N, Mumford E, Nguyen T, Parchariyanon S, Pasick J, Pavade G, Pereda A, Peiris M, Saito T, Swenson S, Van Reeth K, Webby R, Wong F, Ciacci-Zanella J (2014) Review of influenza A virus in swine worldwide: a call for increased surveillance and research. Zoonoses Public Health 61:4–17PubMedCrossRefGoogle Scholar
  71. Virmani N, Bera BC, Singh BK, Shanmugasundaram K, Gulati BR, Barua S, Vaid RK, Gupta AK, Singh RK (2010) Equine influenza outbreak in India (2008–09): virus isolation, sero-epidemiology and phylogenetic analysis of HA gene. Vet Microbiol 143:224–237PubMedCrossRefGoogle Scholar
  72. Waddell GH, Teigland MB, Sigel MM (1963) A new influenza virus associated with equine respiratory disease. J Am Vet Med Assoc 143:587–590PubMedGoogle Scholar
  73. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y (1992) Evolution and ecology of influenza A viruses. Microbiol Rev 56:152–179PubMedPubMedCentralGoogle Scholar
  74. Webster RG, Hinshaw VS, Bean WJ, Van Wyke KL, Geraci JR, St Aubin DJ, Petursson G (1981) Characterization of an influenza A virus from seals. Virology 113:712–724Google Scholar
  75. Webster RG, Peiris JS, Webby RJ, Guan Y (2013) H7N9 Influenza: what we learned from H5N1. Microbe 8:449–505Google Scholar
  76. Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG (1978) Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84:268–278PubMedCrossRefGoogle Scholar
  77. WHO/OIE/FAO H5N1 Evolution Working Group (2014) Revised and updated nomenclature for highly pathogenic avian influenza A (H5N1) viruses. Influenza Other Respir Viruses 8(3):384–388Google Scholar
  78. Zhang Y, Zhang Q, Kong H, Jiang Y, Gao Y, Deng G, Shi J, Tian G, Liu L, Liu J, Guan Y, Bu Z, Chen H (2013) H5N1 hybrid viruses bearing 2009/H1N1 virus genes transmit in guinea pigs by respiratory droplet. Science 340:1459–1463PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Sun-Woo Yoon
    • 1
    • 2
  • Richard J. Webby
    • 1
  • Robert G. Webster
    • 1
    Email author
  1. 1.Division of Virology, Department of Infectious DiseasesSt Jude Children’s Research HospitalMemphisUSA
  2. 2.Viral Infectious Disease Research CenterKorea Research Institute of Bioscience and BiotechnologyDaejeonSouth Korea

Personalised recommendations