Evolutionary Processes in Influenza Viruses: Divergence, Rapid Evolution, and Stasis

  • O. T. Gorman
  • W. J. Bean
  • R. G. Webster
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 176)


Interspecies transmissions combined with isolation of host species contribute to the evolutionary divergence of viruses because of the separation of host-specific virus gene pools. Barriers to frequent interspecies transmissions maintain the separation of progeny and parent virus gene pools and allow independent evolution of host-specific strains. These barriers may be in the form of infrequent likelihood of transmission because of different ecologies of host species, a lack of infectivity of the virus in new hosts, or interference from established viruses mediated by host immunity. Partitioning of avian influenza virus gene pools can result from geographic separation of waterfowl populations by separation of flyways and breeding and overwintering grounds. This mechanism has been suggested for the divergence of H4 hemagglutinin lineages in avian viruses (Donis et al. 1989). The subdivision of host populations provides a great deal of heterogeneity to virus populations and enhances the maintainence of a large number of virus subtypes.


Influenza Virus Avian Influenza Virus Human Influenza Avian Virus Polymerase Acidic 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Air GM, Gibbs AJ, Laver WG, Webster RG (1990) Evolutionary changes in influenza B are not primarily governed by antibody selection. Proc Natl Acad Sci USA 87: 3884–3888PubMedCrossRefGoogle Scholar
  2. Akoto-Amanfu E, Sivasubramanian N, Nayak DP (1987) Primary structure of the polymerase acidic (PA) gene of influenza B virus (B/Sing/22/79). Virology 159: 147–153PubMedCrossRefGoogle Scholar
  3. Altmuller A, Fitch WM, Scholtissek C (1989) Biological and genetic evolution of the nucleoprotein gene of human influenza A viruses. J Gen Virol 70: 2111–2119PubMedCrossRefGoogle Scholar
  4. Bean WJ (1984) Correlation of influenza A virus nucleoprotein genes with host species. Virology 133: 438–442PubMedCrossRefGoogle Scholar
  5. Bean W, Schell M, Gorman O, Kawaoka Y, Katz J, Webster R (1991) Evolution of the H3 influenza virus hemagglutinin from human and non-human hosts. J Virol (in the press)Google Scholar
  6. Becker WB (1966) The isolation and classification of tern virus: influenza virus A/Tern/South Africa/61. J Hyg 64: 309–320CrossRefGoogle Scholar
  7. Both GW, Sleigh MJ, Cox N, Kendal AP (1983) Antigenic drift in influenza virus H3 hemagglutinin from 1968 to 1980: multiple evolutionary pathways and sequential amino acid changes at key antigenic sites. J Virol 48: 52–60PubMedGoogle Scholar
  8. Briedis DJ, Lamb RA (1982) Influenza B virus genome: sequences and structural organization of RNA segment 8 and the mRNAs coding for the NS1 and NS2 proteins. J Virol 42: 186–193PubMedGoogle Scholar
  9. Briedis DJ, Tobin M (1984) Influenza B virus genome: complete nucleotide sequence of the influenza B/Lee/40 virus genome RNA segment 5 encoding the nucleoprotein and comparison with the B/Singapore/222/79 nucleoprotein. Virology 133: 448–455PubMedCrossRefGoogle Scholar
  10. Briedis DJ, Lamb RA, Choppin PW (1982) Sequence of RNA segment 7 of the influenza B virus genome: partial amino acid homology between the membrane proteins ( M1) of influenza A and B viruses and conservation of a second open reading frame. Virology 116: 581–588Google Scholar
  11. Buonagurio D, Nakada S, Desselberger U, Krystal M, Palese P (1985) Noncumulative sequence changes in the hemagglutinin genes of influenza C virus isolates. Virology 146: 221–232PubMedCrossRefGoogle Scholar
  12. Buonagurio DA, Nakada S, Fitch WM, Palese P (1986a) Epidemiology of influenza C virus in man: multiple evolutionary lineages and low rate of change. Virology 153: 12–21PubMedCrossRefGoogle Scholar
  13. Buonagurio DA, Nakada S, Parvin JD, Krystal M, Palese P, Fitch WM (1986b) Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science 232: 980–982PubMedCrossRefGoogle Scholar
  14. Crosby AW (1989) America’s forgotten pandemic, the influenza of 1918. Cambridge University Press, New York, pp 337Google Scholar
  15. Daniels RS, Skehel JJ, Wiley DC (1985) Amino acid sequences of haemagglutinins of influenza viruses of the H3 subtype isolated from horses. J Gen Virol 66: 457–464PubMedCrossRefGoogle Scholar
  16. DeBorde DC, Naeve CW, Herlocher ML, Maassab HF (1987) Nucleotide sequences of the PA and PB1 genes of B/Ann Arbor/1/66 virus: comparison with genes of B/Lee/40 and type A influenza viruses. Virus Res. 8: 33–41PubMedCrossRefGoogle Scholar
  17. Desselberger U, Racariello VR, Zazra JJ, Palese P (1980) The 3’ and 5’-terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene 8: 315–328Google Scholar
  18. Donis RO, Bean WJ, Kawaoka Y, Webster RG (1989) Distinct lineages of influenza virus H4 hemagglutinin genes in different regions of the world. Virology 169: 408–417PubMedCrossRefGoogle Scholar
  19. Frank AL, Taber LH, Glezen WP, Paedes A, Couch RB (1979) Reinfection with influenza A (H3N2) virus in’ young children and their families. J Infect Dis 140: 829–836PubMedCrossRefGoogle Scholar
  20. Frank AL, Taber LH, Wells JM (1983) Individuals infected with two subtypes of influenza A virus in the same season. J Infect Dis 147: 120–124PubMedCrossRefGoogle Scholar
  21. Gammelin M, Altmuller A, Reinhardt U, Mandler J, Harley VR, Hudson PJ, Fitch WM, Scholtissek C (1990) Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th-century avian ancestor. Mol Biol Evol 7: 194–200PubMedGoogle Scholar
  22. Gorman OT, Bean WJ, Kawaoka Y, Webster RG (1990a) Evolution of the nucleoprotein gene of influenza A virus. J Virol 64: 1487–1497PubMedGoogle Scholar
  23. Gorman OT, Donis RO, Kawaoka Y, Webster RG (1990b) Evolution of influenza A virus PB2 genes: implications for evolution of the ribonucleoprotein complex and origin of human influenza A virus. J Virol 64: 4893–4902PubMedGoogle Scholar
  24. Gorman OT, Bean WJ, Kawaoka Y, Donatelli I, Guo Y, Webster RG (1991) Evolution of influenza A virus nucleoprotein genes: implications for the origin of H1 N1 human and classical swine viruses. J Virol 65: 3704–3714PubMedGoogle Scholar
  25. Guo Y, Yin F, Wang P, Wang M, Zhu J (1983) Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus. J Gen Virol 64: 177–182PubMedCrossRefGoogle Scholar
  26. Guo Y, Wang M, Kawaoka Y, Gorman 0, Ito T, Webster RG (1991) Emergence of a new avian-like influenza A virus in horses. Virology (submitted)Google Scholar
  27. Ito T, Gorman O, Kawaoka Y, Bean W, Webster RG (1991) Evolutionary analysis of the influenza A virus M gene with comparison of the M1 and M2 proteins. J Virol 65: 5491–5498PubMedGoogle Scholar
  28. Katagiri S, Ohizumi A, Homma M (1983) An outbreak of type C influenza in a children’s home. J Infect Dis 148: 51–56PubMedCrossRefGoogle Scholar
  29. Kawaoka Y, Gorman OT, Channell DB, Wells KA, Donis RO, Donatelli I, Guo Y, Webster RG (1991) Evolution of the influenza A virus NS gene: Evidence for multiple introductions of human and avian virus genes into pigs. J Virol (submitted)Google Scholar
  30. Kawaoka Y, Gorman OT, Channell DB, Wells KA, Donis RO, Donatelli I, Guo Y, Webster RG (1991) Evolution of the influenza A virus NS gene: Evidence for multiple introductions of human and avian virus genes into pigs. J Virol (submitted)Google Scholar
  31. Kawaoka Y, Yamnikova S, Chambers TM, Lvov DK, Webster RG (1990) Molecular characterization of a new hemagglutinin, subtype H14, of influenza A virus. Virology 179: 759–767PubMedCrossRefGoogle Scholar
  32. Kemdirim S, Palefsky J, Briedis DJ (1986) Influenza B virus PB1 protein: nucleotide sequence of the genome RNA segment predicts a high degree of structural homology with the corresponding influenza A virus polymerase protein. Virology 152: 126–135PubMedCrossRefGoogle Scholar
  33. Kendal AP, Kiley MP (1973) Characterization of influenza virus neuraminidases: peptide changes associated with antigen divergence between early and late N2 neuraminidases. J Virol 12: 1482–1490PubMedGoogle Scholar
  34. Kendal AP, Noble GR, Skehel JJ, Dowdle WR (1978) Antigenic similarity of influenza A (H1 N1) viruses from epidemics in 1977–1978 to “Scandinavian” strains isolated in epidemics of 1950–1951. Virology 89: 632–636PubMedCrossRefGoogle Scholar
  35. Krystal M, Elliott RM, Benz EW, Young JF, Palese P (1982) Evolution of influenza A and B viruses. Conservation of structural features in the hemagglutinin genes. Proc Natl Acad Sci USA 79: 4800–4804Google Scholar
  36. Lamb RA (1983) The influenza virus RNA segments and their encoded proteins. In: Palese P, Kingsbury DW (eds) Genetics of influenza viruses. Springer, Berlin Heidelberg New York, pp 21–69Google Scholar
  37. Lamb RA (1989) Genes and proteins of the influenza viruses. In: Krug RM, Fraenkel-Conrat H, Wagner RR (eds) The influenza viruses. Plenum, New York, pp 1–88Google Scholar
  38. Londo DR, Davis AR, Nayak DP (1983) Complete nucleotide sequence of the nucleoprotein gene of influenza B virus. J Virol 47: 642–648PubMedGoogle Scholar
  39. Mulder J, Masurel N (1958) Pre-epidemic antibody against 1957 strain of Asiatic influenza in serum of older people living in the Netherlands. Lancet 1: 810–814PubMedCrossRefGoogle Scholar
  40. Nakada S, Creager RS, Krystal M, Palese P (1984) Complete nucleotide sequence of the influenza C/California/78 virus nucleoprotein gene. Virus Res 1: 433–441PubMedCrossRefGoogle Scholar
  41. Nakajima K, Desselberger U, Palese P (1978) Recent human influenza A (H1N1) viruses are closely related genetically to strains isolated in 1950. Nature 274: 334–339PubMedCrossRefGoogle Scholar
  42. Nakajima K, Nobusawa E, Nakajima S (1984) Genetic relatedness between A/Swine/lowal/5/30 (H1N1) and human influenza viruses. Virology 139: 194–198PubMedCrossRefGoogle Scholar
  43. O’Callaghan RJ, Gohd RS, Labat DD (1980) Human antibody to influenza C virus: its age-related distribution and distinction from receptor analogs. Infect Immun 30: 500–505PubMedGoogle Scholar
  44. Okazaki K, Kawaoka Y, Webster RG (1989) Evolutionary pathways of the PA genes of influenza A viruses. Virology 172: 601–608PubMedCrossRefGoogle Scholar
  45. Palese P, Young JF (1982) Variation of influenza A, B, and C viruses. Science 215: 1468–1474Google Scholar
  46. Pease CM (1987) An evolutionary epidemiological mechanism, with applications to type A influenza. Theor Popul Biol 31: 422–452PubMedCrossRefGoogle Scholar
  47. Raymond FL, Caton AJ, Cox NJ, Kendal AP, Brownlee GG (1986) The antigenicity and evolution of influenza H1 haemagglutinin from 1950–1957 and 1977–1983: two pathways from one gene. Virology 148: 275–287PubMedCrossRefGoogle Scholar
  48. Scholtissek C, Rohde W, von Hoyningen V, Rott R (1978) On the origin of the human influenza virus subtypes H2N2 and H3N2. Virology 87: 13–20PubMedCrossRefGoogle Scholar
  49. Scholtissek C, Burger H, Bachmann PA, Hannoun C (1983) Genetic relatedness of hemagglutinins of the H1 subtype of influenza A viruses isolated from swine and birds. Virology 129: 521–523PubMedCrossRefGoogle Scholar
  50. Scholtissek C, Burger H, Kistner O, Shortridge KF (1985) The nucleoprotein as a possible major factor in determining host specificity of influenza H3N2 viruses. Virology 147: 287–294PubMedCrossRefGoogle Scholar
  51. Shaw MW, Lamb RA, Erickson BW, Briedis DJ, Choppin PW (1982) Complete nucleotide sequence of the neuraminidase gene of influenza B virus. Proc Nall Acad Sci USA 79: 6817–6821CrossRefGoogle Scholar
  52. Sivasubramanian N, Nayak DP (1982) Sequence analysis of the polymerase 1 gene and the secondary structure prediction of polymerase 1 protein of human influenza virus A/WSN/33. J Virol 44: 321–329PubMedGoogle Scholar
  53. Smith FI, Palese P (1989) Variation in influenza virus genes. In: Krug RM (ed) The influenza viruses. Plenum, New York, pp 319–359Google Scholar
  54. Snyder MH, Buckler-White AJ, London WT, Tierney EL, Murphy BR (1987) The avian influenza virus nucleoprotein gene and a specific constellation of avian and human virus polymerase genes each specify attenuation of avian/human influenza A/Pintail/79 reassortant viruses from monkeys. J Virol 61: 2857–2863PubMedGoogle Scholar
  55. Tian SF, Buckler-White AJ, London WT, Reck LJ, Channock RM, Murphy BR (1985) Nucleoprotein and membrane protein genes are associated with restriction of replication of influenza A/Mallard/NY/78 virus and its reassortants in squirrel monkey respiratory tract. J Virology 53: 771–775PubMedGoogle Scholar
  56. Treanor JJ, Snyder MH, London WT, Murphy BR (1989) The B allele of the NS gene of avian influenza viruses, but not the A allele, attenuates a human influenza A virus for squirrel monkeys. Virology 171: 1–9PubMedCrossRefGoogle Scholar
  57. Webster RG, Laver WG (1975) Antigenic variation of influenza viruses. In: Kilbourne ED (ed) The influenza viruses and influenza. Academic, New York, pp 269–314Google Scholar
  58. Webster RG, Yakhno MA, Hinshaw VS, Bean WJ, Murti KG (1978) Intestinal influenza: replication and characterization of influenza viruses in ducks. Virology 84: 268–278PubMedCrossRefGoogle Scholar
  59. Webster RG, Kawaoka Y, Bean WJ (1989) What is the potential of avirulent influenza viruses to complement a cleavable hemagglutinin and generate virulent strains? Virology 171: 484–492PubMedCrossRefGoogle Scholar
  60. Yamashita M, Krystal M, Fitch WM, Palese P (1988) Influenza B virus evolution: co-circulating lineages and comparison of evolutionary pattern with those of influenza A and C viruses. Virology 163: 112–122PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin · Heidelberg 1992

Authors and Affiliations

  • O. T. Gorman
    • 1
  • W. J. Bean
    • 1
  • R. G. Webster
    • 1
  1. 1.Department of Virology and Molecular BiologySt. Jude Children’s Research HospitalMemphisUSA

Personalised recommendations