Skip to main content
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
. 1995 Jun 20;92(13):5841–5844. doi: 10.1073/pnas.92.13.5841

Exponential increases of RNA virus fitness during large population transmissions.

I S Novella 1, E A Duarte 1, S F Elena 1, A Moya 1, E Domingo 1, J J Holland 1
PMCID: PMC41597  PMID: 7597039

Abstract

The great adaptability shown by RNA viruses is a consequence of their high mutation rates. Here we investigate the kinetics of virus fitness gains during repeated transfers of large virus populations in cell culture. Results always show that fitness increases exponentially. Low fitness clones exhibit regular increases observed as biphasic periods of exponential evolutionary improvement, while neutral clones show monophasic kinetics. These results are significant for RNA virus epidemiology, optimal handling of attenuated live virus vaccines, and routine laboratory procedures.

Full text

PDF
5841

Selected References

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

  1. Bennett A. F., Dao K. M., Lenski R. E. Rapid evolution in response to high-temperature selection. Nature. 1990 Jul 5;346(6279):79–81. doi: 10.1038/346079a0. [DOI] [PubMed] [Google Scholar]
  2. Chao L. Fitness of RNA virus decreased by Muller's ratchet. Nature. 1990 Nov 29;348(6300):454–455. doi: 10.1038/348454a0. [DOI] [PubMed] [Google Scholar]
  3. Clarke D. K., Duarte E. A., Elena S. F., Moya A., Domingo E., Holland J. The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci U S A. 1994 May 24;91(11):4821–4824. doi: 10.1073/pnas.91.11.4821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Clarke D. K., Duarte E. A., Moya A., Elena S. F., Domingo E., Holland J. Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J Virol. 1993 Jan;67(1):222–228. doi: 10.1128/jvi.67.1.222-228.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Coffin J. M. Genetic diversity and evolution of retroviruses. Curr Top Microbiol Immunol. 1992;176:143–164. doi: 10.1007/978-3-642-77011-1_10. [DOI] [PubMed] [Google Scholar]
  6. Domingo E., Escarmis C., Martinez M. A., Martinez-Salas E., Mateu M. G. Foot-and-mouth disease virus populations are quasispecies. Curr Top Microbiol Immunol. 1992;176:33–47. doi: 10.1007/978-3-642-77011-1_3. [DOI] [PubMed] [Google Scholar]
  7. Drake J. W. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160–7164. doi: 10.1073/pnas.88.16.7160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drake J. W. Rates of spontaneous mutation among RNA viruses. Proc Natl Acad Sci U S A. 1993 May 1;90(9):4171–4175. doi: 10.1073/pnas.90.9.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Duarte E. A., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. Many-trillionfold amplification of single RNA virus particles fails to overcome the Muller's ratchet effect. J Virol. 1993 Jun;67(6):3620–3623. doi: 10.1128/jvi.67.6.3620-3623.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. Subclonal components of consensus fitness in an RNA virus clone. J Virol. 1994 Jul;68(7):4295–4301. doi: 10.1128/jvi.68.7.4295-4301.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Duarte E. A., Novella I. S., Weaver S. C., Domingo E., Wain-Hobson S., Clarke D. K., Moya A., Elena S. F., de la Torre J. C., Holland J. J. RNA virus quasispecies: significance for viral disease and epidemiology. Infect Agents Dis. 1994 Aug;3(4):201–214. [PubMed] [Google Scholar]
  12. Duarte E., Clarke D., Moya A., Domingo E., Holland J. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6015–6019. doi: 10.1073/pnas.89.13.6015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eigen M. Viral quasispecies. Sci Am. 1993 Jul;269(1):42–49. doi: 10.1038/scientificamerican0793-42. [DOI] [PubMed] [Google Scholar]
  14. Haigh J. The accumulation of deleterious genes in a population--Muller's Ratchet. Theor Popul Biol. 1978 Oct;14(2):251–267. doi: 10.1016/0040-5809(78)90027-8. [DOI] [PubMed] [Google Scholar]
  15. Holland J. J., de la Torre J. C., Clarke D. K., Duarte E. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol. 1991 Jun;65(6):2960–2967. doi: 10.1128/jvi.65.6.2960-2967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. Rapid evolution of RNA genomes. Science. 1982 Mar 26;215(4540):1577–1585. doi: 10.1126/science.7041255. [DOI] [PubMed] [Google Scholar]
  17. Lefrancios L., Lyles D. S. The interactionof antiody with the major surface glycoprotein of vesicular stomatitis virus. I. Analysis of neutralizing epitopes with monoclonal antibodies. Virology. 1982 Aug;121(1):157–167. [PubMed] [Google Scholar]
  18. Lefrancois L., Lyles D. S. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology. 1982 Aug;121(1):168–174. doi: 10.1016/0042-6822(82)90126-x. [DOI] [PubMed] [Google Scholar]
  19. Lenski R. E., Travisano M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6808–6814. doi: 10.1073/pnas.91.15.6808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lynch M., Bürger R., Butcher D., Gabriel W. The mutational meltdown in asexual populations. J Hered. 1993 Sep-Oct;84(5):339–344. doi: 10.1093/oxfordjournals.jhered.a111354. [DOI] [PubMed] [Google Scholar]
  21. MULLER H. J. THE RELATION OF RECOMBINATION TO MUTATIONAL ADVANCE. Mutat Res. 1964 May;106:2–9. doi: 10.1016/0027-5107(64)90047-8. [DOI] [PubMed] [Google Scholar]
  22. Martell M., Esteban J. I., Quer J., Genescà J., Weiner A., Esteban R., Guardia J., Gómez J. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J Virol. 1992 May;66(5):3225–3229. doi: 10.1128/jvi.66.5.3225-3229.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mudd J. A., Summers D. F. Protein synthesis in vesicular stomatitis virus-infected HeLa cells. Virology. 1970 Oct;42(2):328–340. doi: 10.1016/0042-6822(70)90277-1. [DOI] [PubMed] [Google Scholar]
  24. Novella I. S., Elena S. F., Moya A., Domingo E., Holland J. J. Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol. 1995 May;69(5):2869–2872. doi: 10.1128/jvi.69.5.2869-2872.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Strauss J. H., Strauss E. G. Evolution of RNA viruses. Annu Rev Microbiol. 1988;42:657–683. doi: 10.1146/annurev.mi.42.100188.003301. [DOI] [PubMed] [Google Scholar]
  26. Wimmer E., Hellen C. U., Cao X. Genetics of poliovirus. Annu Rev Genet. 1993;27:353–436. doi: 10.1146/annurev.ge.27.120193.002033. [DOI] [PubMed] [Google Scholar]
  27. Wright S. Evolution in Mendelian Populations. Genetics. 1931 Mar;16(2):97–159. doi: 10.1093/genetics/16.2.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de la Torre J. C., Holland J. J. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol. 1990 Dec;64(12):6278–6281. doi: 10.1128/jvi.64.12.6278-6281.1990. [DOI] [PMC free article] [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