Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1993 Jun;67(6):3620–3623. doi: 10.1128/jvi.67.6.3620-3623.1993

Many-trillionfold amplification of single RNA virus particles fails to overcome the Muller's ratchet effect.

E A Duarte 1, D K Clarke 1, A Moya 1, S F Elena 1, E Domingo 1, J Holland 1
PMCID: PMC237712  PMID: 8388514

Abstract

We showed earlier that transfers of large populations of RNA viruses lead to fitness gains and that repeated genetic bottleneck transfers result in fitness losses due to Muller's ratchet. In the present study, we examined the effects of genetic bottleneck passages intervening between population passages, a process akin to some natural viral transmissions, using vesicular stomatitis virus as a model. Our findings show that the pronounced fitness increases that occur during two successive population passages cannot overcome the fitness decreases caused by a single intervening genetic bottleneck passage. The implications for natural transmissions of RNA viruses are discussed.

Full text

PDF
3620

Selected References

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

  1. Artenstein M. S., Miller W. S. Air sampling for respiratory disease agents in army recruits. Bacteriol Rev. 1966 Sep;30(3):571–572. doi: 10.1128/br.30.3.571-572.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bilsel P. A., Nichol S. T. Polymerase errors accumulating during natural evolution of the glycoprotein gene of vesicular stomatitis virus Indiana serotype isolates. J Virol. 1990 Oct;64(10):4873–4883. doi: 10.1128/jvi.64.10.4873-4883.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. 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]
  4. Chao L. Levels of selection, evolution of sex in RNA viruses, and the origin of life. J Theor Biol. 1991 Nov 21;153(2):229–246. doi: 10.1016/s0022-5193(05)80424-2. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. 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]
  7. Coffin J. M. Genetic variation in AIDS viruses. Cell. 1986 Jul 4;46(1):1–4. doi: 10.1016/0092-8674(86)90851-2. [DOI] [PubMed] [Google Scholar]
  8. Couch R. B., Cate T. R., Douglas R. G., Jr, Gerone P. J., Knight V. Effect of route of inoculation on experimental respiratory viral disease in volunteers and evidence for airborne transmission. Bacteriol Rev. 1966 Sep;30(3):517–529. doi: 10.1128/br.30.3.517-529.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DE JONG J. G., WINKLER K. C. SURVIVAL OF MEASLES VIRUS IN AIR. Nature. 1964 Mar 7;201:1054–1055. doi: 10.1038/2011054a0. [DOI] [PubMed] [Google Scholar]
  10. Domingo E., Holland J. J. Complications of RNA heterogeneity for the engineering of virus vaccines and antiviral agents. Genet Eng (N Y) 1992;14:13–31. doi: 10.1007/978-1-4615-3424-2_2. [DOI] [PubMed] [Google Scholar]
  11. Domingo E., Martínez-Salas E., Sobrino F., de la Torre J. C., Portela A., Ortín J., López-Galindez C., Pérez-Breña P., Villanueva N., Nájera R. The quasispecies (extremely heterogeneous) nature of viral RNA genome populations: biological relevance--a review. Gene. 1985;40(1):1–8. doi: 10.1016/0378-1119(85)90017-4. [DOI] [PubMed] [Google Scholar]
  12. Domingo E. RNA virus evolution and the control of viral disease. Prog Drug Res. 1989;33:93–133. doi: 10.1007/978-3-0348-9146-2_5. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Dykhuizen D., Hartl D. L. Selective neutrality of 6PGD allozymes in E. coli and the effects of genetic background. Genetics. 1980 Dec;96(4):801–817. doi: 10.1093/genetics/96.4.801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. ENDERS J. F., KATZ S. L., MILOVANOVIC M. V., HOLLOWAY A. Studies on an attenuated measles-virus vaccine. I. Development and preparations of the vaccine: technics for assay of effects of vaccination. N Engl J Med. 1960 Jul 28;263:153–159. doi: 10.1056/NEJM196007282630401. [DOI] [PubMed] [Google Scholar]
  16. Elena S. F., González-Candelas F., Moya A. Does the VP1 gene of foot-and-mouth disease virus behave as a molecular clock? J Mol Evol. 1992 Sep;35(3):223–229. doi: 10.1007/BF00178598. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. 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]
  19. Gerone P. J., Couch R. B., Keefer G. V., Douglas R. G., Derrenbacher E. B., Knight V. Assessment of experimental and natural viral aerosols. Bacteriol Rev. 1966 Sep;30(3):576–588. doi: 10.1128/br.30.3.576-588.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gorman O. T., Bean W. J., Webster R. G. Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis. Curr Top Microbiol Immunol. 1992;176:75–97. doi: 10.1007/978-3-642-77011-1_6. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. Holmes E. C., Zhang L. Q., Simmonds P., Ludlam C. A., Brown A. J. Convergent and divergent sequence evolution in the surface envelope glycoprotein of human immunodeficiency virus type 1 within a single infected patient. Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):4835–4839. doi: 10.1073/pnas.89.11.4835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kinnunen L., Pöyry T., Hovi T. Genetic diversity and rapid evolution of poliovirus in human hosts. Curr Top Microbiol Immunol. 1992;176:49–61. doi: 10.1007/978-3-642-77011-1_4. [DOI] [PubMed] [Google Scholar]
  26. Kondrashov A. S. Deleterious mutations and the evolution of sexual reproduction. Nature. 1988 Dec 1;336(6198):435–440. doi: 10.1038/336435a0. [DOI] [PubMed] [Google Scholar]
  27. Kurath G., Palukaitis P. Serial passage of infectious transcripts of a cucumber mosaic virus satellite RNA clone results in sequence heterogeneity. Virology. 1990 May;176(1):8–15. doi: 10.1016/0042-6822(90)90224-f. [DOI] [PubMed] [Google Scholar]
  28. Lee C. M., Bih F. Y., Chao Y. C., Govindarajan S., Lai M. M. Evolution of hepatitis delta virus RNA during chronic infection. Virology. 1992 May;188(1):265–273. doi: 10.1016/0042-6822(92)90756-f. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Lefrancois L., Lyles D. S. Antigenic determinants of vesicular stomatitis virus: analysis with antigenic variants. J Immunol. 1983 Jan;130(1):394–398. [PubMed] [Google Scholar]
  31. 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]
  32. 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]
  33. 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]
  34. 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]
  35. Nee S. Deleterious mutation and genetic recombination. Nature. 1988 Jan 28;331(6154):308–308. doi: 10.1038/331308a0. [DOI] [PubMed] [Google Scholar]
  36. Nee S. On the evolution of sex in RNA viruses. J Theor Biol. 1989 Jun 8;138(3):407–412. doi: 10.1016/s0022-5193(89)80201-2. [DOI] [PubMed] [Google Scholar]
  37. Nowak M. A., Anderson R. M., McLean A. R., Wolfs T. F., Goudsmit J., May R. M. Antigenic diversity thresholds and the development of AIDS. Science. 1991 Nov 15;254(5034):963–969. doi: 10.1126/science.1683006. [DOI] [PubMed] [Google Scholar]
  38. Rojas E. R., Carrillo E., Schiappacassi M., Campos R. Modification of foot-and-mouth disease virus O1 Caseros after serial passages in the presence of antiviral polyclonal sera. J Virol. 1992 Jun;66(6):3368–3372. doi: 10.1128/jvi.66.6.3368-3372.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Sacramento D., Badrane H., Bourhy H., Tordo N. Molecular epidemiology of rabies virus in France: comparison with vaccine strains. J Gen Virol. 1992 May;73(Pt 5):1149–1158. doi: 10.1099/0022-1317-73-5-1149. [DOI] [PubMed] [Google Scholar]
  40. Smith D. B., Inglis S. C. The mutation rate and variability of eukaryotic viruses: an analytical review. J Gen Virol. 1987 Nov;68(Pt 11):2729–2740. doi: 10.1099/0022-1317-68-11-2729. [DOI] [PubMed] [Google Scholar]
  41. Steinhauer D. A., Domingo E., Holland J. J. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene. 1992 Dec 15;122(2):281–288. doi: 10.1016/0378-1119(92)90216-c. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. 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]
  44. 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]
  45. Wain-Hobson S. Human immunodeficiency virus type 1 quasispecies in vivo and ex vivo. Curr Top Microbiol Immunol. 1992;176:181–193. doi: 10.1007/978-3-642-77011-1_12. [DOI] [PubMed] [Google Scholar]
  46. Ward C. D., Flanegan J. B. Determination of the poliovirus RNA polymerase error frequency at eight sites in the viral genome. J Virol. 1992 Jun;66(6):3784–3793. doi: 10.1128/jvi.66.6.3784-3793.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev. 1992 Mar;56(1):152–179. doi: 10.1128/mr.56.1.152-179.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Wechsler D. S., Dang C. V. Opposite orientations of DNA bending by c-Myc and Max. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7635–7639. doi: 10.1073/pnas.89.16.7635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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 Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES