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. 1996 Mar;142(3):673–679. doi: 10.1093/genetics/142.3.673

Evolution of Fitness in Experimental Populations of Vesicular Stomatitis Virus

S F Elena 1, F Gonzalez-Candelas 1, I S Novella 1, E A Duarte 1, D K Clarke 1, E Domingo 1, J J Holland 1, A Moya 1
PMCID: PMC1207009  PMID: 8849878

Abstract

The evolution of fitness in experimental clonal populations of vesicular stomatitis virus (VSV) has been compared under different genetic (fitness of initial clone) and demographic (population dynamics) regimes. In spite of the high genetic heterogeneity among replicates within experiments, there is a clear effect of population dynamics on the evolution of fitness. Those populations that went through strong periodic bottlenecks showed a decreased fitness in competition experiments with wild type. Conversely, mutant populations that were transferred under the dynamics of continuous population expansions increased their fitness when compared with the same wild type. The magnitude of the observed effect depended on the fitness of the original viral clone. Thus, high fitness clones showed a larger reduction in fitness than low fitness clones under dynamics with included periodic bottleneck. In contrast, the gain in fitness was larger the lower the initial fitness of the viral clone. The quantitative genetic analysis of the trait ``fitness'' in the resulting populations shows that genetic variation for the trait is positively correlated with the magnitude of the change in the same trait. The results are interpreted in terms of the operation of MULLER's ratchet and genetic drift as opposed to the appearance of beneficial mutations.

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Selected References

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  1. 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]
  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. 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]
  5. Delassus S., Cheynier R., Wain-Hobson S. Evolution of human immunodeficiency virus type 1 nef and long terminal repeat sequences over 4 years in vivo and in vitro. J Virol. 1991 Jan;65(1):225–231. doi: 10.1128/jvi.65.1.225-231.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Domingo E., Sabo D., Taniguchi T., Weissmann C. Nucleotide sequence heterogeneity of an RNA phage population. Cell. 1978 Apr;13(4):735–744. doi: 10.1016/0092-8674(78)90223-4. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. Fitch W. M., Leiter J. M., Li X. Q., Palese P. Positive Darwinian evolution in human influenza A viruses. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4270–4274. doi: 10.1073/pnas.88.10.4270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gillespie J. H. Episodic evolution of RNA viruses. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10411–10412. doi: 10.1073/pnas.90.22.10411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. 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]
  13. 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]
  14. Holland J. J., De La Torre J. C., Steinhauer D. A. RNA virus populations as quasispecies. Curr Top Microbiol Immunol. 1992;176:1–20. doi: 10.1007/978-3-642-77011-1_1. [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. J., de la Torre J. C., Steinhauer D. A., Clarke D., Duarte E., Domingo E. Virus mutation frequencies can be greatly underestimated by monoclonal antibody neutralization of virions. J Virol. 1989 Dec;63(12):5030–5036. doi: 10.1128/jvi.63.12.5030-5036.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Marich J. E., Pontsler A. V., Rice S. M., McGraw K. A., Dubensky T. W. The phylogenetic relationship and complete nucleotide sequence of human papillomavirus type 35. Virology. 1992 Feb;186(2):770–776. doi: 10.1016/0042-6822(92)90045-q. [DOI] [PubMed] [Google Scholar]
  20. Martínez M. A., Dopazo J., Hernández J., Mateu M. G., Sobrino F., Domingo E., Knowles N. J. Evolution of the capsid protein genes of foot-and-mouth disease virus: antigenic variation without accumulation of amino acid substitutions over six decades. J Virol. 1992 Jun;66(6):3557–3565. doi: 10.1128/jvi.66.6.3557-3565.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nichol S. T., Rowe J. E., Fitch W. M. Punctuated equilibrium and positive Darwinian evolution in vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10424–10428. doi: 10.1073/pnas.90.22.10424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Steinhauer D. A., Holland J. J. Direct method for quantitation of extreme polymerase error frequencies at selected single base sites in viral RNA. J Virol. 1986 Jan;57(1):219–228. doi: 10.1128/jvi.57.1.219-228.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Steinhauer D. A., Holland J. J. Rapid evolution of RNA viruses. Annu Rev Microbiol. 1987;41:409–433. doi: 10.1146/annurev.mi.41.100187.002205. [DOI] [PubMed] [Google Scholar]
  24. Steinhauer D. A., de la Torre J. C., Holland J. J. High nucleotide substitution error frequencies in clonal pools of vesicular stomatitis virus. J Virol. 1989 May;63(5):2063–2071. doi: 10.1128/jvi.63.5.2063-2071.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Stephan W., Chao L., Smale J. G. The advance of Muller's ratchet in a haploid asexual population: approximate solutions based on diffusion theory. Genet Res. 1993 Jun;61(3):225–231. doi: 10.1017/s0016672300031384. [DOI] [PubMed] [Google Scholar]
  26. Vandepol S. B., Lefrancois L., Holland J. J. Sequences of the major antibody binding epitopes of the Indiana serotype of vesicular stomatitis virus. Virology. 1986 Jan 30;148(2):312–325. doi: 10.1016/0042-6822(86)90328-4. [DOI] [PubMed] [Google Scholar]
  27. White B. T., McGeoch D. J. Isolation and characterization of conditional lethal amber nonsense mutants of vesicular stomatitis virus. J Gen Virol. 1987 Dec;68(Pt 12):3033–3044. doi: 10.1099/0022-1317-68-12-3033. [DOI] [PubMed] [Google Scholar]

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