Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 May 15;88(10):4270–4274. doi: 10.1073/pnas.88.10.4270

Positive Darwinian evolution in human influenza A viruses.

W M Fitch 1, J M Leiter 1, X Q Li 1, P Palese 1
PMCID: PMC51640  PMID: 1840695

Abstract

We earlier suggested that type A human influenza virus genes undergo positive Darwinian selection through immune surveillance. This requires more favorable amino acid replacements fixed in antigenic sites among the surviving lineages than among the extinct lineages. We now show that viral hemagglutinins fix proportionately more amino acid replacements in antigenic sites in the trunk of the evolutionary tree (survivors) than in the branches (nonsurvivors), demonstrating that type A human influenza virus is undergoing positive Darwinian evolution. The hemagglutinin gene is evolving 3 times faster than the nonstructural gene and the average age of the sampled nonsurvivors is only 1.6 years, so that extinction is not only common but rapid.

Full text

PDF
4270

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. ATWOOD K. C., SCHNEIDER L. K., RYAN F. J. Periodic selection in Escherichia coli. Proc Natl Acad Sci U S A. 1951 Mar;37(3):146–155. doi: 10.1073/pnas.37.3.146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Air G. M., Gibbs A. J., Laver W. G., Webster R. G. Evolutionary changes in influenza B are not primarily governed by antibody selection. Proc Natl Acad Sci U S A. 1990 May;87(10):3884–3888. doi: 10.1073/pnas.87.10.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Both G. W., Sleigh M. J., Cox N. J., Kendal A. P. 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. 1983 Oct;48(1):52–60. doi: 10.1128/jvi.48.1.52-60.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Buonagurio D. A., Nakada S., Parvin J. D., Krystal M., Palese P., Fitch W. M. Evolution of human influenza A viruses over 50 years: rapid, uniform rate of change in NS gene. Science. 1986 May 23;232(4753):980–982. doi: 10.1126/science.2939560. [DOI] [PubMed] [Google Scholar]
  5. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974 Oct;78(2):737–756. doi: 10.1093/genetics/78.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gammelin M., Altmüller A., Reinhardt U., Mandler J., Harley V. R., Hudson P. J., Fitch W. M., Scholtissek C. Phylogenetic analysis of nucleoproteins suggests that human influenza A viruses emerged from a 19th-century avian ancestor. Mol Biol Evol. 1990 Mar;7(2):194–200. doi: 10.1093/oxfordjournals.molbev.a040594. [DOI] [PubMed] [Google Scholar]
  7. Gojobori T., Moriyama E. N., Kimura M. Molecular clock of viral evolution, and the neutral theory. Proc Natl Acad Sci U S A. 1990 Dec;87(24):10015–10018. doi: 10.1073/pnas.87.24.10015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hauptmann R., Clarke L. D., Mountford R. C., Bachmayer H., Almond J. W. Nucleotide sequence of the haemagglutinin gene of influenza virus A/England/321/77. J Gen Virol. 1983 Jan;64(Pt 1):215–220. doi: 10.1099/0022-1317-64-1-215. [DOI] [PubMed] [Google Scholar]
  9. Hayashida H., Toh H., Kikuno R., Miyata T. Evolution of influenza virus genes. Mol Biol Evol. 1985 Jul;2(4):289–303. doi: 10.1093/oxfordjournals.molbev.a040352. [DOI] [PubMed] [Google Scholar]
  10. Hughes A. L., Nei M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A. 1989 Feb;86(3):958–962. doi: 10.1073/pnas.86.3.958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
  12. Kawaoka Y., Bean W. J., Webster R. G. Evolution of the hemagglutinin of equine H3 influenza viruses. Virology. 1989 Apr;169(2):283–292. doi: 10.1016/0042-6822(89)90153-0. [DOI] [PubMed] [Google Scholar]
  13. Laskowski M., Jr, Kato I., Kohr W. J., Park S. J., Tashiro M., Whatley H. E. Positive darwinian selection in evolution of protein inhibitors of serine proteinases. Cold Spring Harb Symp Quant Biol. 1987;52:545–553. doi: 10.1101/sqb.1987.052.01.062. [DOI] [PubMed] [Google Scholar]
  14. Newton S. E., Air G. M., Webster R. G., Laver W. G. Sequence of the hemagglutinin gene of influenza virus A/Memphis/1/71 and previously uncharacterized monoclonal antibody-derived variants. Virology. 1983 Jul 30;128(2):495–501. doi: 10.1016/0042-6822(83)90277-5. [DOI] [PubMed] [Google Scholar]
  15. Palese P., Young J. F. Variation of influenza A, B, and C viruses. Science. 1982 Mar 19;215(4539):1468–1474. doi: 10.1126/science.7038875. [DOI] [PubMed] [Google Scholar]
  16. Ratner V. A., Kolchanov N. A., Omel'ianchuk L. V. Filogeneticheskii analiz genov virusa grippa. Sootnoshenie adaptivnosti i neitral'nosti. Genetika. 1989 Aug;25(8):1499–1507. [PubMed] [Google Scholar]
  17. Raymond F. L., Caton A. J., Cox N. J., Kendal A. P., Brownlee G. G. The antigenicity and evolution of influenza H1 haemagglutinin, from 1950-1957 and 1977-1983: two pathways from one gene. Virology. 1986 Jan 30;148(2):275–287. doi: 10.1016/0042-6822(86)90325-9. [DOI] [PubMed] [Google Scholar]
  18. Saitou N., Nei M. Polymorphism and evolution of influenza A virus genes. Mol Biol Evol. 1986 Jan;3(1):57–74. doi: 10.1093/oxfordjournals.molbev.a040381. [DOI] [PubMed] [Google Scholar]
  19. Sleigh M. J., Both G. W., Underwood P. A., Bender V. J. Antigenic drift in the hemagglutinin of the Hong Kong influenza subtype: correlation of amino acid changes with alterations in viral antigenicity. J Virol. 1981 Mar;37(3):845–853. doi: 10.1128/jvi.37.3.845-853.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Stewart C. B., Schilling J. W., Wilson A. C. Adaptive evolution in the stomach lysozymes of foregut fermenters. 1987 Nov 26-Dec 2Nature. 330(6146):401–404. doi: 10.1038/330401a0. [DOI] [PubMed] [Google Scholar]
  21. Sugita S., Yoshioka Y., Itamura S., Kanegae Y., Oguchi K., Gojobori T., Nerome K., Oya A. Molecular evolution of hemagglutinin genes of H1N1 swine and human influenza A viruses. J Mol Evol. 1991 Jan;32(1):16–23. doi: 10.1007/BF02099924. [DOI] [PubMed] [Google Scholar]
  22. Verhoeyen M., Fang R., Jou W. M., Devos R., Huylebroeck D., Saman E., Fiers W. Antigenic drift between the haemagglutinin of the Hong Kong influenza strains A/Aichi/2/68 and A/Victoria/3/75. Nature. 1980 Aug 21;286(5775):771–776. doi: 10.1038/286771a0. [DOI] [PubMed] [Google Scholar]
  23. Webster R. G., Laver W. G., Air G. M., Schild G. C. Molecular mechanisms of variation in influenza viruses. Nature. 1982 Mar 11;296(5853):115–121. doi: 10.1038/296115a0. [DOI] [PubMed] [Google Scholar]
  24. Weis W., Brown J. H., Cusack S., Paulson J. C., Skehel J. J., Wiley D. C. Structure of the influenza virus haemagglutinin complexed with its receptor, sialic acid. Nature. 1988 Jun 2;333(6172):426–431. doi: 10.1038/333426a0. [DOI] [PubMed] [Google Scholar]
  25. Wiley D. C., Skehel J. J. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus. Annu Rev Biochem. 1987;56:365–394. doi: 10.1146/annurev.bi.56.070187.002053. [DOI] [PubMed] [Google Scholar]
  26. Wiley D. C., Wilson I. A., Skehel J. J. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature. 1981 Jan 29;289(5796):373–378. doi: 10.1038/289373a0. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES