Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2006;299:51–82. doi: 10.1007/3-540-26397-7_3

Viruses as Quasispecies: Biological Implications

E Domingo 2, V Martín 2, C Perales 2, A Grande-Pérez 2, J García-Arriaza 2, A Arias 2
Editor: Esteban Domingo1
PMCID: PMC7120838  PMID: 16568896

Abstract

During viral infections, the complex and dynamic distributions of variants, termed viral quasispecies, play a key role in the adaptability of viruses to changing environments and the fate of the population as a whole. Mutant spectra are continuously and avoidably generated during RNA genome replication, and they are not just a by-product of error-prone replication, devoid of biological relevance. On the contrary, current evidence indicates that mutant spectra contribute to viral pathogenesis, can modulate the expression of phenotypic traits by subpopulations of viruses, can include memory genomes that reflect the past evolutionary history of the viral lineage, and, furthermore, can participate in viral extinction through lethal mutagenesis. Also, mutant spectra are the target on which selection and random drift act to shape the long-term evolution of viruses. The biological relevance of mutant spectra is the central topic of this chapter.

Keywords: Vesicular Stomatitis Virus, Mutant Spectrum, Biological Implication, Lymphocytic Choriomeningitis Virus, Mutant Distribution

Contributor Information

Esteban Domingo, Email: edomingo@cbm.uam.es.

E. Domingo, Email: edomingo@cbm.uam.es

References

  1. Agol V.I. Picornavirus genetics: an overview. In: Semler B.L., Wimmer E., editors. Molecular biology of picornaviruses. Washington DC: American Society for Microbiology; 2002. pp. 269–284. [Google Scholar]
  2. Airaksinen A., Pariente N., Menendez-Arias L., Domingo E. Curing of foot-and-mouth disease virus from persistently infected cellsby ribavirin involves enhanced mutagenesis. Virology. 2003;311:339–349. doi: 10.1016/S0042-6822(03)00144-2. [DOI] [PubMed] [Google Scholar]
  3. Anderson J.P., Daifuku R., Loeb L.A. Viral error catastrophe by mutagenic nucleosides. Annu Rev Microbiol. 2004;58:183–205. doi: 10.1146/annurev.micro.58.030603.123649. [DOI] [PubMed] [Google Scholar]
  4. Arias A, Agudo R, Ferrer-Orta C, Pérez-Luque R, Airaksinen A, Brocchi E, Domingo E, Verdaguer N, Escarmis C (2005) Mutant viral polymerase in the transition of virus to error catastrophe identifies a critical site for RNA binding. J Mol Biol (in press) [DOI] [PubMed]
  5. Arias A., Lázaro E., Escarmís C., Domingo E. Molecular intermediates of fitness gain of an RNA virus: characterization of a mutant spectrum by biological and molecular cloning. J Gen Virol. 2001;82:1049–1060. doi: 10.1099/0022-1317-82-5-1049. [DOI] [PubMed] [Google Scholar]
  6. Arias A., Ruiz-Jarabo C.M., Escarmis C., Domingo E. Fitness increase of memory genomes in a viral quasispecies. J Mol Biol. 2004;339:405–412. doi: 10.1016/j.jmb.2004.03.061. [DOI] [PubMed] [Google Scholar]
  7. Baranowski E., Ruíz-Jarabo C.M., Pariente N., Verdaguer N., Domingo E. Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv Virus Res. 2003;62:19–111. doi: 10.1016/S0065-3527(03)62002-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bergstrom C.T., McElhany P., Real L.A. Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci U S A. 1999;96:5095–5100. doi: 10.1073/pnas.96.9.5095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Biebricher C.K. Mutation, competition and selection as measured with small RNA molecules. In: Domingo E., Webster R.G., Holland J.J., editors. Origin and evolution of viruses. San Diego: Academic Press; 1999. pp. 65–85. [Google Scholar]
  10. Borrego B., Novella I.S., Giralt E., Andreu D., Domingo E. Distinct repertoire of antigenic variants of foot-and-mouth disease virus in the presence or absence of immune selection. J Virol. 1993;67:6071–6079. doi: 10.1128/jvi.67.10.6071-6079.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Borrow P., Lewicki H., Wei X., Horwitz M.S., Peffer N., Meyers H., Nelson J.A., Gairin J.E., Hahn B.H., Oldstone M.B., Shaw G.M. Antiviral pressure exerted by HIV-1-specific cytotoxic T lymphocytes (CTLs) during primary infection demonstrated by rapid selection of CTL escape virus. Nat Med. 1997;3:205–211. doi: 10.1038/nm0297-205. [DOI] [PubMed] [Google Scholar]
  12. Briones C., Mas A., Gómez-Mariano G., Altisent C., Menéndez-Arias L., Soriano V., Domingo E. Dynamics of dominance of a dipeptide insertion in reverse transcriptase of HIV-1 from patients subjected to prolonged therapy. Virus Res. 2000;66:13–26. doi: 10.1016/S0168-1702(99)00120-3. [DOI] [PubMed] [Google Scholar]
  13. Briones C., Domingo E., Molina-París C. Memory in retroviral quasispecies: experimental evidence and theoretical model for human immunodeficiency virus. J Mol Biol. 2003;331:213–229. doi: 10.1016/S0022-2836(03)00661-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Charpentier C., Dwyer D.E., Mammano F., Lecossier D., Clavel F., Hance A.J. Role of minority populations of human immunodeficiency virus type 1 in the evolution of viral resistance to protease inhibitors. J Virol. 2004;78:4234–4247. doi: 10.1128/JVI.78.8.4234-4247.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Chumakov K.M., Powers L.B., Noonan K.E., Roninson I.B., Levenbook I.S. Correlation between amount of virus with altered nucleotide sequence and the monkey test for acceptability of oral poliovirus vaccine. Proc Natl Acad Sci U S A. 1991;88:199–203. doi: 10.1073/pnas.88.1.199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Coffin J.M. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science. 1995;267:483–489. doi: 10.1126/science.7824947. [DOI] [PubMed] [Google Scholar]
  17. Condit C. Principles of virology. In: Knipe D.M., Howley P.M., editors. Fields virology. Philadelphia: Lippincot Williams and Wilkins; 2001. pp. 811–815. [Google Scholar]
  18. Contreras A.M., Hiasa Y., He W., Terella A., Schmidt E.V., Chung R.T. Viral RNA mutations are region specific and increased by ribavirin in a full-length hepatitis C virus replication system. J Virol. 2002;76:8505–8517. doi: 10.1128/JVI.76.17.8505-8517.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Cornell C.T., Brunner J.E., Semler B.L. Differential rescue of poliovirus RNA replication functions by genetically modified RNA polymerase precursors. J Virol. 2004;78:13007–13018. doi: 10.1128/JVI.78.23.13007-13018.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Cowan G.A., Pines D., Meltzer D., editors. Complexity. Metaphors, models and reality. The Advanced Book Program, Jacob Way. Reading, MA: Addison-Wesley Publishing; 1994. [Google Scholar]
  21. Crotty S., Maag D., Arnold J.J., Zhong W., Lau J.Y.N., Hong Z., Andino R., Cameron C.E. The broad-spectrum antiviral ribonucleotide, ribavirin, is an RNA virus mutagen. Nat Med. 2000;6:1375–1379. doi: 10.1038/82191. [DOI] [PubMed] [Google Scholar]
  22. De la Torre J.C., Holland J.J. RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol. 1990;64:6278–6281. doi: 10.1128/jvi.64.12.6278-6281.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Crotty S., Cameron C.E., Andino R. RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A. 2001;98:6895–6900. doi: 10.1073/pnas.111085598. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. DeFilippis V.R., Villarreal L.P. An introduction to the evolutionary ecology of viruses. In: Hurst C.J., editor. Viral ecology. San Diego: Academic Press; 2000. pp. 125–208. [Google Scholar]
  25. Dobzhansky T. Nothing in biology makes sense except in the light of evolution. Am Biol Teacher. 1973;35:125–129. [Google Scholar]
  26. Domingo E. Biological significance of viral quasispecies. Viral Hepatitis Reviews. 1996;2:247–261. [Google Scholar]
  27. Domingo E. RNA virus evolution, population dynamics, and nutritional status. Biol Trace Elem Res. 1997;56:23–30. doi: 10.1007/BF02778981. [DOI] [PubMed] [Google Scholar]
  28. Domingo E. Quasispecies. In: Granoff A., Webster R.G., editors. Encyclopedia of virology. London: Academic Press; 1999. pp. 1431–1436. [Google Scholar]
  29. Domingo E. Viruses at the edge of adaptation. Virology. 2000;270:251–253. doi: 10.1006/viro.2000.0320. [DOI] [PubMed] [Google Scholar]
  30. Domingo E. Quasispecies and the development of new antiviral strategies. Prog Drug Res. 2003;60:133–158. doi: 10.1007/978-3-0348-8012-1_4. [DOI] [PubMed] [Google Scholar]
  31. Domingo E. Microbial evolution and emerging diseases. In: Power C., Johnson R.T., editors. Emerging neurological infections. New York: Marcel Dekker; 2005. [Google Scholar]
  32. Domingo E. Virus entry into error catastrophe as a new antiviral strategy. 2005;107:115–228. [Google Scholar]
  33. Domingo E., Holland J.J. RNA virus mutations and fitness for survival. Annu Rev Microbiol. 1997;51:151–178. doi: 10.1146/annurev.micro.51.1.151. [DOI] [PubMed] [Google Scholar]
  34. Domingo E., Holland J.J., Biebricher C., Eigen M. Quasispecies: the concept and the word. In: Gibbs A., Calisher C., García-Arenal F., editors. Molecular evolution of the viruses. Cambridge: Cambridge University Press; 1995. pp. 171–180. [Google Scholar]
  35. Domingo E, Biebricher C, Eigen M, Holland JJ (2001) Quasispecies and RNA virus evolution: principles and consequences. Austin, Landes Bioscience
  36. Domingo E., Ruíz-Jarabo C.M., Arias A., Molina-Paris C., Briones C., Baranowski E., Escarmís C. Detection and biological implications of genetic memory in viral quasispecies. In: Matsumori A., editor. Cardiomyopathies and heart failure: biomolecular, infectious and immune mechanisms. London: Kluwer; 2003. pp. 259–276. [Google Scholar]
  37. Domingo E., Brun A., Núñez J.I., Cristina J., Briones C., Escarmís C. Genomics of viruses. In: Hacker J., Dobrindt U., editors. Pathogenomics: Genome Analysis of Pathogenic Microbes. Weinheim: WILEY-VCH Verlag GmbH and Co.KGaA; 2006. pp. 369–388. [Google Scholar]
  38. Drake J.W., Holland J.J. Mutation rates among RNA viruses. Proc Natl Acad Sci U S A. 1999;96:13910–13913. doi: 10.1073/pnas.96.24.13910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Eastman P.S., Blair C.D. Temperature-sensitive mutants of Japanese encephalitis virus. J Virol. 1985;55:611–616. doi: 10.1128/jvi.55.3.611-616.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Eigen M. Self-organization of matter and the evolution of biological macromolecules. Naturwissenschaften. 1971;58:465–523. doi: 10.1007/BF00623322. [DOI] [PubMed] [Google Scholar]
  41. Eigen M. Steps towards life. Oxford: Oxford University Press; 1992. [Google Scholar]
  42. Eigen M. Error catastrophe and antiviral strategy. Proc Natl Acad Sci U S A. 2002;99:13374–13376. doi: 10.1073/pnas.212514799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Eigen M., Schuster P. The hypercycle. A principle of natural self-organization. Berlin Heidelberg New York: Springer; 1979. [DOI] [PubMed] [Google Scholar]
  44. Eigen M., Biebricher C.K. Sequence space and quasispecies distribution. In: Domingo E., Ahlquist P., Holland J.J., editors. RNA genetics. Boca Raton, FL: CRC Press; 1988. pp. 211–245. [Google Scholar]
  45. Escarmís C., Dávila M., Charpentier N., Bracho A., Moya A., Domingo E. Genetic lesions associated with Muller’s ratchet in an RNA virus. J Mol Biol. 1996;264:255–267. doi: 10.1006/jmbi.1996.0639. [DOI] [PubMed] [Google Scholar]
  46. Flint S.J., Enquist L.W., Racaniello V.R., Skalka A.M. Principles of virology. Molecular biology, pathogenesis, and control of animal viruses. Washington, DC: ASMPress; 2004. [Google Scholar]
  47. Frank S.A. The design of natural and artificial adaptive systems. In: Rose M.R., Lauder G.V., editors. Adaptation. San Diego: Academic; 1996. pp. 451–505. [Google Scholar]
  48. Freistadt M.S., Meades G.D., Cameron C.E. Lethal mutagens: broad-spectrum antivirals with limited potential for development of resistance? Drug Resist Updat. 2004;7:19–24. doi: 10.1016/j.drup.2003.12.003. [DOI] [PubMed] [Google Scholar]
  49. García-Lerma J.G., Nidtha S., Blumoff K., Weinstock H., Heneine W. Increased ability for selection of zidovudine resistance in a distinct class of wild-type HIV-1 from drug-naive persons. Proc Natl Acad Sci U S A. 2001;98:13907–13912. doi: 10.1073/pnas.241300698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. García-Arriaza J., Manrubia S.C., Toja M., Domingo E., Escarmís C. Evolutionary transition toward defective RNAs that are infectious by complementation. J Virol. 2004;78:11678–11685. doi: 10.1128/JVI.78.21.11678-11685.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. García-Arriaza J., Domingo E., Escarmís C. A segmented form of foot-and-mouth disease virus interferes with standard virus: a link between interference and competitive fitness. Virology. 2005;335:155–164. doi: 10.1016/j.virol.2005.02.012. [DOI] [PubMed] [Google Scholar]
  52. Gell-Mann M. Complex adaptive systems. In: Cowan G.A., Pines D., Meltzer D., editors. Complexity metaphors, models and reality. Reading, MA: Wesley; 1994. pp. 17–45. [Google Scholar]
  53. Gerrish P.J., Garcia-Lerma J.G. Mutation rate and the efficacy of antimicrobial drug treatment. The Lancet Infect Dis. 2003;3:28–32. doi: 10.1016/s1473-3099(03)00485-7. [DOI] [PubMed] [Google Scholar]
  54. González-López C., Gómez-Mariano G., Escarmís C., Domingo E. Invariant aphthovirus consensus nucleotide sequence in the transition to error catastrophe. Infect Genet Evol. 2005;5:366–374. doi: 10.1016/j.meegid.2005.05.001. [DOI] [PubMed] [Google Scholar]
  55. González-López C., Arias A., Pariente N., Gómez-Mariano G., Domingo E. Preextinction viral RNA can interfere with infectivity. J Virol. 2004;78:3319–3324. doi: 10.1128/JVI.78.7.3319-3324.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Graci J.D., Cameron C.E. Quasispecies, error catastrophe, and the antiviral activity of ribavirin. Virology. 2002;298:175–180. doi: 10.1006/viro.2002.1487. [DOI] [PubMed] [Google Scholar]
  57. Grande-Pérez A., Sierra S., Castro M.G., Domingo E., Lowenstein P.R. Molecular indetermination in the transition to error catastrophe: systematic elimination of lymphocytic choriomeningitis virus through mutagenesis does not correlate linearly with large increases in mutant spectrum complexity. Proc Natl Acad Sci U S A. 2002;99:12938–12943. doi: 10.1073/pnas.182426999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Grande-Pérez A., Lázaro E., Lowenstein P., Domingo E., Manrubia S.C. Suppression of viral infectivity through lethal defection. Proc Natl Acad Sci U S A. 2005;102:4448–4452. doi: 10.1073/pnas.0408871102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Grande-Pérez A., Gómez-Mariano G., Lowenstein P., Domingo E. Mutagenesis-induced, large fitness variations with an invariant arenavirus consensus genomic nucleotide sequence. J Virol. 2005;79:10451–10459. doi: 10.1128/JVI.79.16.10451-10459.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Holland J.J. Defective viral genomes. In: Fields B.M., Knipe D.M., editors. Virology. New York: Raven; 1990. pp. 151–165. [Google Scholar]
  61. Holland J.J., Domingo E., de la Torre J.C., Steinhauer D.A. Mutation frequencies at defined single codon sites in vesicular stomatitis virus and poliovirus can be increased only slightly by chemical mutagenesis. J Virol. 1990;64:3960–3962. doi: 10.1128/jvi.64.8.3960-3962.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. 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;65:2960–2967. doi: 10.1128/jvi.65.6.2960-2967.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Huang A.S., Baltimore D. Defective viral particles and viral disease processes. Nature. 1970;226:325–327. doi: 10.1038/226325a0. [DOI] [PubMed] [Google Scholar]
  64. Imamichi H., Crandall K.A., Natarajan V., Jiang M.K., Dewar R.L., Berg S., Gaddam A., Bosche M., Metcalf J.A., Davey R.T., Jr, Lane H.C. Human immunodeficiency virus type 1 quasi species that rebound after discontinuation of highly active antiretroviral therapy are similar to the viral quasi species present before initiation of therapy. J Infect Dis. 2001;183:36–50. doi: 10.1086/317641. [DOI] [PubMed] [Google Scholar]
  65. Karlsson A.C., Gaines H., Sallberg M., Lindback S., Sonnerborg A. Reappearance of founder virus sequence in human immunodeficiency virus type 1-infected patients. J Virol. 1999;73:6191–6196. doi: 10.1128/jvi.73.7.6191-6196.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Kijak G.H., Simon V., Balfe P., Vanderhoeven J., Pampuro S.E., Zala C., Ochoa C., Cahn P., Markowitz M., Salomon H. Origin of human immunodeficiency virus type 1 quasispecies emerging after antiretroviral treatment interruption in patients with therapeutic failure. J Virol. 2002;76:7000–7009. doi: 10.1128/JVI.76.14.7000-7009.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Lanford R.E., Chavez D., Guerra B., Lau J.Y., Hong Z., Brasky K.M., Beames B. Ribavirin induces error-prone replication of GB virus B in primary tamarin hepatocytes. J Virol. 2001;75:8074–8081. doi: 10.1128/JVI.75.17.8074-8081.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Lau D.T., Khokhar M.F., Doo E., Ghany M.G., Herion D., Park Y., Kleiner D.E., Schmid P., Condreay L.D., Gauthier J., Kuhns M.C., Liang T.J., Hoofnagle J.H. Long-term therapy of chronic hepatitis B with lamivudine. Hepatology. 2000;32:828–834. doi: 10.1053/jhep.2000.17912. [DOI] [PubMed] [Google Scholar]
  69. Lee C.H., Gilbertson D.L., Novella I.S., Huerta R., Domingo E., Holland J.J. Negative effects of chemical mutagenesis on the adaptive behavior of vesicular stomatitis virus. J Virol. 1997;71:3636–3640. doi: 10.1128/jvi.71.5.3636-3640.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Lewontin R.C. The units of selection. Annu Rev Ecol System. 1970;1:1–18. [Google Scholar]
  71. Loeb L.A., Mullins J.I. Lethal mutagenesis of HIV by mutagenic ribonucleoside analogs. AIDS Res Hum Retroviruses. 2000;13:1–3. doi: 10.1089/088922200309539. [DOI] [PubMed] [Google Scholar]
  72. Loeb L.A., Essigmann J.M., Kazazi F., Zhang J., Rose K.D., Mullins J.I. Lethal mutagenesis of HIV with mutagenic nucleoside analogs. Proc Natl Acad Sci U S A. 1999;96:1492–1497. doi: 10.1073/pnas.96.4.1492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Maag D., Castro C., Hong Z., Cameron C.E. Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as amediator of the antiviral activity of ribavirin. J Biol Chem. 2001;276:46094–46098. doi: 10.1074/jbc.C100349200. [DOI] [PubMed] [Google Scholar]
  74. Mahy BWJ (ed) (2005) Foot-and-mouth disease virus. Curr Topics Microbiol Immunol 288 [DOI] [PubMed]
  75. McHutchison J.G., Gordon S.C., Schiff E.R., Shiffman M.L., Lee W.M., Rustgi V.K., Goodman Z.D., Ling M.H., Cort S., Albrecht J.K. Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. N Engl J Med. 1998;339:1485–1492. doi: 10.1056/NEJM199811193392101. [DOI] [PubMed] [Google Scholar]
  76. Miralles R., Gerrish P.J., Moya A., Elena S.F. Clonal interference and the evolution of RNA viruses. Science. 1999;285:1745–1747. doi: 10.1126/science.285.5434.1745. [DOI] [PubMed] [Google Scholar]
  77. Moreno I.M., Malpica J.M., Rodriguez-Cerezo E., Garcia-Arenal F. A mutation in tomato aspermy cucumovirus that abolishes cell-to-cell movement is maintained to high levels in the viral RNA population by complementation. J Virol. 1997;71:9157–9162. doi: 10.1128/jvi.71.12.9157-9162.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Mount D.W. Bioinformatics. sequence and genome analysis. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 2004. [Google Scholar]
  79. Nájera I., Holguín A., Quiñones-Mateu M.E., Muñoz-Fernández M.A., Nájera R., López-Galíndez C., Domingo E. Pol gene quasispecies of human immunodeficiency virus: mutations associated with drug resistance in virus from patients undergoing no drug therapy. J Virol. 1995;69:23–3. doi: 10.1128/jvi.69.1.23-31.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Novella I.S. Contributions of vesicular stomatitis virus to the understanding of RNA virus evolution. Curr Opin Microbiol. 2003;6:399–405. doi: 10.1016/S1369-5274(03)00084-5. [DOI] [PubMed] [Google Scholar]
  81. Novella I.S. Negative effect of genetic bottlenecks on the adaptability of vesicular stomatitis virus. J Mol Biol. 2004;336:61–67. doi: 10.1016/j.jmb.2003.12.002. [DOI] [PubMed] [Google Scholar]
  82. 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;69:2869–2872. doi: 10.1128/jvi.69.5.2869-2872.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Novella I.S., Quer J., Domingo E., Holland J.J. Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J Virol. 1999;73:1668–1671. doi: 10.1128/jvi.73.2.1668-1671.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Novella I.S., Reissig D.D., Wilke C.O. Density-dependent selection in vesicular stomatitis virus. J Virol. 2004;78:5799–5804. doi: 10.1128/JVI.78.11.5799-5804.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Nowak M., Schuster P. Error thresholds of replication in finite populations mutation frequencies and the onset of Muller’s ratchet. J Theor Biol. 1989;137:375–395. doi: 10.1016/s0022-5193(89)80036-0. [DOI] [PubMed] [Google Scholar]
  86. Nowak M.A., May R.M. Virus dynamics. Mathematical principles of immunology and virology. New York: Oxford University Press; 2000. [Google Scholar]
  87. Oldstone M.B.A. Biology and pathogenesis of lymphocytic choriomeningitis virus infection. Curr Top Microbiol Immunol. 2002;263:83–117. doi: 10.1007/978-3-642-56055-2_6. [DOI] [PubMed] [Google Scholar]
  88. Pariente N., Sierra S., Lowenstein P.R., Domingo E. Efficient virus extinction by combinations of a mutagen and antiviral inhibitors. J Virol. 2001;75:9723–9730. doi: 10.1128/JVI.75.20.9723-9730.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Parker W.B., Cheng Y.C. Metabolism and mechanism of action of 5-fluorouracil. Pharmacol Ther. 1990;48:381–395. doi: 10.1016/0163-7258(90)90056-8. [DOI] [PubMed] [Google Scholar]
  90. Perales C., Martin V., Ruiz-Jarabo C.M., Domingo E. Monitoring sequence space as a test for the target of selection in viruses. J Mol Biol. 2005;345:451–459. doi: 10.1016/j.jmb.2004.10.066. [DOI] [PubMed] [Google Scholar]
  91. Perrault J. Origin and replication of defective interfering particles. Curr Top Microbiol Immunol. 1981;93:151–207. doi: 10.1007/978-3-642-68123-3_7. [DOI] [PubMed] [Google Scholar]
  92. Pringle C.R. Genetic characteristics of conditional lethal mutants of vesicular stomatitis virus induced by 5-fluorouracil, 5-azacytidine, and ethyl methane sulfonate. J Virol. 1970;5:559–567. doi: 10.1128/jvi.5.5.559-567.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. Quiñones-Mateu M.E., Arts E.J. HIV-1 fitness: implications for drug resistance, disease progression, and global epidemic evolution. In: Kuiken C., Foley B., Hahn B.H., Marx P., McCutchan F.E., Mellors J., Mullins J.I., Sodroski J., Wolinsky S., Korber B.T., editors. HIV-1 sequence compendium. Los Alamos NM: Los Alamos National Laboratory; 2002. pp. 134–170. [Google Scholar]
  94. Ribeiro R.M., Bonhoeffer S., Nowak M.A. The frequency of resistant mutant virus before antiviral therapy. AIDS. 1998;26:461–465. doi: 10.1097/00002030-199805000-00006. [DOI] [PubMed] [Google Scholar]
  95. Rowlands DJ. Foot-and-mouth disease. Virus Res. 2003;91:1–161. doi: 10.1016/s0168-1702(02)00259-9. [DOI] [PubMed] [Google Scholar]
  96. Ruiz-Jarabo C.M., Arias A., Baranowski E., Escarmís C., Domingo E. Memory in viral quasispecies. J Virol. 2000;74:3543–3547. doi: 10.1128/JVI.74.8.3543-3547.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  97. Ruiz-Jarabo C.M., Arias A., Molina-París C., Briones C., Baranowski E., Escarmís C., Domingo E. Duration and fitness dependence of quasispecies memory. J Mol Biol. 2002;315:285–296. doi: 10.1006/jmbi.2001.5232. [DOI] [PubMed] [Google Scholar]
  98. Ruiz-Jarabo C.M., Ly C., Domingo E., de la Torre J.C. Lethal mutagenesis of the prototypic arenavirus lymphocytic choriomeningitis virus (LCMV) Virology. 2003;308:37–47. doi: 10.1016/S0042-6822(02)00046-6. [DOI] [PubMed] [Google Scholar]
  99. Ruiz-Jarabo C.M., Miller E., Gómez-Mariano G., Domingo E. Synchronous loss of quasispecies memory in parallel viral lineages: a deterministic feature of viral quasispecies. J Mol Biol. 2003;333:553–563. doi: 10.1016/j.jmb.2003.08.054. [DOI] [PubMed] [Google Scholar]
  100. Severson W.E., Schmaljohn C.S., Javadian A., Jonsson C.B. Ribavirin causes error catastrophe during Hantaan virus replication. J Virol. 2003;77:481–488. doi: 10.1128/JVI.77.1.481-488.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Sierra S., Dávila M., Lowenstein P.R., Domingo E. Response of foot-and-mouth disease virus to increased mutagenesis. Influence of viral load and fitness in loss of infectivity. J Virol. 2000;74:8316–8323. doi: 10.1128/JVI.74.18.8316-8323.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  102. Simmonds P., Smith D.B. Structural constraints on RNA virus evolution. J Virol. 1999;73:5787–5794. doi: 10.1128/jvi.73.7.5787-5794.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  103. Simmonds P., Tuplin A., Evans D.J. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA. 2004;10:1337–1351. doi: 10.1261/rna.7640104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Smolinski M.S., Hamburg M.A., Lederberg J., editors. Microbial threats to health. Emergence, detection and response. Washington, DC: The National Academies Press; 2003. [PubMed] [Google Scholar]
  105. Snell N.J. Ribavirin—current status of a broad spectrum antiviral agent. Expert Opin Pharmacother. 2001;2:1317–1324. doi: 10.1517/14656566.2.8.1317. [DOI] [PubMed] [Google Scholar]
  106. Snijder E.J., Bredenbeek P.J., Dobbe J.C., Thiel V., Ziebuhr J., Poon L.L., Guan Y., Rozanov M., Spaan W.J., Gorbalenya A.E. Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol. 2003;331:991–1004. doi: 10.1016/S0022-2836(03)00865-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Sobrino F., Domingo E., editors. Foot-and-mouth disease: current perspectives. Wymondham, UK: Horizon Bioscience; 2004. [Google Scholar]
  108. Solé R., Goodwin B. Signs of life. how complexity pervedes biology. New York: Basic Books; 2000. [Google Scholar]
  109. Swetina J., Schuster P. Self-replication with errors. A model for polynucleotide replication. Biophys Chem. 1982;16:329–345. doi: 10.1016/0301-4622(82)87037-3. [DOI] [PubMed] [Google Scholar]
  110. Teng M.N., Oldstone M.B., de la Torre J.C. Suppression of lymphocytic choriomeningitis virus-induced growth hormone deficiency syndrome by diseasenegative virus variants. Virology. 1996;223:113–119. doi: 10.1006/viro.1996.0460. [DOI] [PubMed] [Google Scholar]
  111. Turner P.E., Chao L. Sex and the evolution of intrahost competition in RNA virus phi6. Genetics. 1998;150:523–532. doi: 10.1093/genetics/150.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  112. Vo N.V., Young K.C., Lai M.M.C. Mutagenic and inhibitory effects of ribavirin on hepatitis C virus RNA polymerase. Biochemistry. 2003;42:10462–10471. doi: 10.1021/bi0344681. [DOI] [PubMed] [Google Scholar]
  113. Volkenstein M.V. Physical approaches to biological evolution. Berlin Heidelberg New York: Springer-Verlag; 1994. [Google Scholar]
  114. Welsh C. Antibiotics. Actions, origins, resistance. Washington, DC: ASM Press; 2003. [Google Scholar]
  115. White D.O., Fenner F.J. Medical virology. Orlando, FL: Academic; 1986. [Google Scholar]
  116. Wilke C.O., Reissig D.D., Novella I.S. Replication at periodically changing multiplicity of infection promotes stable coexistence of competing viral populations. Evolution Int J Org Evolution. 2004;58:900–905. doi: 10.1111/j.0014-3820.2004.tb00422.x. [DOI] [PubMed] [Google Scholar]
  117. Williams G.C. Natural selection. Domains, levels and challenges. New York: Oxford University Press; 1992. [Google Scholar]
  118. Woese C.R. A new biology for a new century. Microbiol Mol Biol Reviews. 2004;68:173–186. doi: 10.1128/MMBR.68.2.173-186.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  119. Woolhouse M.E.J. Mathematical models of the epidemiology and control of foot-and-mouth disease. In: Sobrino F., Domingo E., editors. Foot and mouth disease current perspectives. Wymondham UK: Horizon Bioscience; 2004. pp. 355–381. [Google Scholar]
  120. Wyatt C.A., Andrus L., Brotman B., Huang F., Lee D.H., Prince A.M. Immunity in chimpanzees chronically infected with hepatitis C virus: role of minor quasispecies in reinfection. J Virol. 1998;72:1725–1730. doi: 10.1128/jvi.72.3.1725-1730.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Youngner J.S., Whitaker-Dowling P. Interference. In: Granoff A., Webster R.G., editors. Encyclopedia of virology. San Diego: Academic Press; 1999. pp. 850–854. [Google Scholar]

Articles from Quasispecies: Concept and Implications for Virology are provided here courtesy of Nature Publishing Group

RESOURCES