1887

Journal of General Virology header logo

Volume 94, Issue 4

The role of environmental factors on the evolution of phenotypic diversity in vesicular stomatitis virus populations Free

Abstract

Virus adaptation to an ever-changing environment requires the availability of variants with phenotypes that can fulfil new requirements for replication. High mutation rates result in the generation of these variants. The factors that contribute to the maintenance or elimination of this diversity, however, are not fully understood. This study used a collection of vesicular stomatitis virus strains generated under different conditions to measure the extent of variation within each population, and tested the effects of several environmental factors on diversity. It was found that the host-cell type used for selection sometimes had an effect on the extent of variation and that there may be different levels of variation over time. Persistent infections promoted higher levels of diversity than acute infections, presumably due to complementation. In contrast, environmental heterogeneity, host breadth and the cell type used for testing (as opposed to the cell type used for selection) did not seem to have an effect on the amount of phenotypic diversity observed.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.048082-0
2013-04-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/4/860.html?itemId=/content/journal/jgv/10.1099/vir.0.048082-0&mimeType=html&fmt=ahah

References

  1. Ali A., Roossinck M. J. 2010; Genetic bottlenecks during systemic movement of Cucumber mosaic virus vary in different host plants. Virology 404:279–283 [View Article][PubMed]
     [Google Scholar]
  2. Atwood K. C., Schneider L. K., Ryan F. J. 1951; Periodic selection in Escherichia coli . Proc Natl Acad Sci U S A 37:146–155 [View Article][PubMed]
     [Google Scholar]
  3. Badyaev A. V. 2009; Evolutionary significance of phenotypic accommodation in novel environments: an empirical test of the Baldwin effect. Philos Trans R Soc Lond B Biol Sci 364:1125–1141 [View Article][PubMed]
     [Google Scholar]
  4. Brown M. B., Forsythe A. B. 1974; Robust tests for equality of variances. J Am Stat Assoc 69:364–367 [View Article]
     [Google Scholar]
  5. Buckling A., Wills M. A., Colegrave N. 2003; Adaptation limits diversification of experimental bacterial populations. Science 302:2107–2109 [View Article][PubMed]
     [Google Scholar]
  6. Ciota A. T., Kramer L. D. 2010; Insights into arbovirus evolution and adaptation from experimental studies. Viruses 2:2594–2617 [View Article][PubMed]
     [Google Scholar]
  7. Ciota A. T., Ngo K. A., Lovelace A. O., Payne A. F., Zhou Y., Shi P.-Y., Kramer L. D. 2007; Role of the mutant spectrum in adaptation and replication of West Nile virus. J Gen Virol 88:865–874 [View Article][PubMed]
     [Google Scholar]
  8. Ciota A. T., Lovelace A. O., Jia Y., Davis L. J., Young D. S., Kramer L. D. 2008; Characterization of mosquito-adapted West Nile virus. J Gen Virol 89:1633–1642 [View Article][PubMed]
     [Google Scholar]
  9. Ciota A. T., Jia Y., Payne A. F., Jerzak G., Davis L. J., Young D. S., Ehrbar D., Kramer L. D. 2009; Experimental passage of St. Louis encephalitis virus in vivo in mosquitoes and chickens reveals evolutionarily significant virus characteristics. PLoS ONE 4:e7876 [View Article][PubMed]
     [Google Scholar]
  10. Ciota A. T., Koch E. M., Willsey G. G., Davis L. J., Jerzak G. V., Ehrbar D. J., Wilke C. O., Kramer L. D. 2011; Temporal and spatial alterations in mutant swarm size of St. Louis encephalitis virus in mosquito hosts. Infect Genet Evol 11:460–468 [View Article][PubMed]
     [Google Scholar]
  11. Ciota A. T., Ehrbar D. J., Van Slyke G. A., Payne A. F., Willsey G. G., Viscio R. E., Kramer L. D. 2012a; Quantification of intrahost bottlenecks of West Nile virus in Culex pipiens mosquitoes using an artificial mutant swarm. Infect Genet Evol 12:557–564 [View Article][PubMed]
     [Google Scholar]
  12. Ciota A. T., Ehrbar D. J., Van Slyke G. A., Willsey G. G., Kramer L. D. 2012b; Cooperative interactions in the West Nile virus mutant swarm. BMC Biol Evol 12:58 [View Article]
     [Google Scholar]
  13. Coffey L. L., Vignuzzi M. 2011; Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J Virol 85:1025–1035 [View Article][PubMed]
     [Google Scholar]
  14. Cuevas J. M., Moya A., Elena S. F. 2003; Evolution of RNA virus in spatially structured heterogeneous environments. J Evol Biol 16:456–466 [View Article][PubMed]
     [Google Scholar]
  15. Delassus S., Cheynier R., Wain-Hobson S. 1992; Nonhomogeneous distribution of human immunodeficiency virus type 1 proviruses in the spleen. J Virol 66:5642–5645[PubMed]
     [Google Scholar]
  16. Domingo E., Holland J. J. 1997; RNA virus mutations and fitness for survival. Annu Rev Microbiol 51:151–178 [View Article][PubMed]
     [Google Scholar]
  17. Domingo E., Sheldon J., Perales C. 2012; Viral quasispecies evolution. Microbiol Mol Biol Rev 76:159–216 [View Article][PubMed]
     [Google Scholar]
  18. Drake J. W., Holland J. J. 1999; Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913 [View Article][PubMed]
     [Google Scholar]
  19. Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. 1994a; Subclonal components of consensus fitness in an RNA virus clone. J Virol 68:4295–4301[PubMed]
     [Google Scholar]
  20. 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. 1994b; RNA virus quasispecies: significance for viral disease and epidemiology. Infect Agents Dis 3:201–214[PubMed]
     [Google Scholar]
  21. Dutta R. N., Rouzine I. M., Smith S. D., Wilke C. O., Novella I. S. 2008; Rapid adaptive amplification of preexisting variation in an RNA virus. J Virol 82:4354–4362 [View Article][PubMed]
     [Google Scholar]
  22. Elena S. F., Miralles R., Moya A. 1997; Frequency-dependent selection in a mammalian RNA virus. Evolution 51:984–987 [View Article]
     [Google Scholar]
  23. Frost S. D. W., Dumaurier M. J., Wain-Hobson S., Brown A. J. L. 2001; Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc Natl Acad Sci U S A 98:6975–6980 [View Article][PubMed]
     [Google Scholar]
  24. Gause G. F. 2003 The Struggle for Existence, Dover Edn. Mineola, NY: Dover Publications;
     [Google Scholar]
  25. Holland J. J., de la Torre J. C., Clarke D. K., Duarte E. 1991; Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65:2960–2967[PubMed]
     [Google Scholar]
  26. Jasmin J. N., Kassen R. 2007; Evolution of a single niche specialist in variable environments. Proc Biol Sci 274:2761–2767 [View Article][PubMed]
     [Google Scholar]
  27. Jerzak G. V., Bernard K., Kramer L. D., Shi P.-Y., Ebel G. D. 2007; The West Nile virus mutant spectrum is host-dependant and a determinant of mortality in mice. Virology 360:469–476 [View Article][PubMed]
     [Google Scholar]
  28. Jerzak G. V., Brown I., Shi P.-Y., Kramer L. D., Ebel G. D. 2008; Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374:256–260 [View Article][PubMed]
     [Google Scholar]
  29. Jridi C., Martin J.-F., Marie-Jeanne V., Labonne G., Blanc S. 2006; Distinct viral populations differentiate and evolve independently in a single perennial host plant. J Virol 80:2349–2357 [View Article][PubMed]
     [Google Scholar]
  30. Kassen R. 2002; The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190 [View Article]
     [Google Scholar]
  31. Kassen R., Rainey P. B. 2004; The ecology and genetics of microbial diversity. Annu Rev Microbiol 58:207–231 [View Article][PubMed]
     [Google Scholar]
  32. Lefrancois L., Lyles D. S. 1982; The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. I. Analysis of neutralizing epitopes with monoclonal antibodies. Virology 121:157–167 [View Article][PubMed]
     [Google Scholar]
  33. Li H., Roossinck M. J. 2004; Genetic bottlenecks reduce population variation in an experimental RNA virus population. J Virol 78:10582–10587 [View Article][PubMed]
     [Google Scholar]
  34. Notley-McRobb L., Ferenci T. 2000; Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. Genetics 156:1493–1501[PubMed]
     [Google Scholar]
  35. Novella I. S., Duarte E. A., Elena S. F., Moya A., Domingo E., Holland J. J. 1995; Exponential increases of RNA virus fitness during large population transmissions. Proc Natl Acad Sci U S A 92:5841–5844 [View Article][PubMed]
     [Google Scholar]
  36. Novella I. S., Hershey C. L., Escarmis C., Domingo E., Holland J. J. 1999a; Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287:459–465 [View Article][PubMed]
     [Google Scholar]
  37. Novella I. S., Quer J., Domingo E., Holland J. J. 1999b; Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J Virol 73:1668–1671[PubMed]
     [Google Scholar]
  38. Novella I. S., Reissig D. D., Wilke C. O. 2004; Density-dependent selection in vesicular stomatitis virus. J Virol 78:5799–5804 [View Article][PubMed]
     [Google Scholar]
  39. Novella I. S., Ebendick-Corpus B. E., Zárate S., Miller E. L. 2007; Emergence of mammalian cell-adapted vesicular stomatitis virus from persistent infections of insect vector cells. J Virol 81:6664–6668 [View Article][PubMed]
     [Google Scholar]
  40. Novella I. S., Presloid J. B., Zhou T., Smith-Tsurkan S. D., Ebendick-Corpus B. E., Dutta R. N., Lust K. L., Wilke C. O. 2010; Genomic evolution of vesicular stomatitis virus strains with differences in adaptability. J Virol 84:4960–4968 [View Article][PubMed]
     [Google Scholar]
  41. Novella I. S., Presloid J. B., Smith S. D., Wilke C. O. 2011; Specific and nonspecific host adaptation during arboviral experimental evolution. J Mol Microbiol Biotechnol 21:71–81 [View Article][PubMed]
     [Google Scholar]
  42. Presloid J. B., Ebendick-Corpus B. E., Zárate S., Novella I. S. 2008; Antagonistic pleiotropy involving promoter sequences in a virus. J Mol Biol 382:342–352 [View Article][PubMed]
     [Google Scholar]
  43. Rainey P. B., Travisano M. 1998; Adaptive radiation in a heterogeneous environment. Nature 394:69–72 [View Article][PubMed]
     [Google Scholar]
  44. Rainey P. B., Buckling A., Kassen R., Travisano M. 2000; The emergence and maintenance of diversity: insights from experimental bacterial populations. Trends Ecol Evol 15:243–247 [View Article][PubMed]
     [Google Scholar]
  45. Remold S. K., Rambaut A., Turner P. E. 2008; Evolutionary genomics of host adaptation in vesicular stomatitis virus. Mol Biol Evol 25:1138–1147 [View Article][PubMed]
     [Google Scholar]
  46. Sanjuán R., Nebot M. R., Chirico N., Mansky L. M., Belshaw R. 2010; Viral mutation rates. J Virol 84:9733–9748 [View Article][PubMed]
     [Google Scholar]
  47. Saxer G., Doebeli M., Travisano M. 2009; Spatial structure leads to ecological breakdown and loss of diversity. Proc Biol Sci 276:2065–2070 [View Article][PubMed]
     [Google Scholar]
  48. Schneider W. L., Roossinck M. J. 2000; Evolutionarily related Sindbis-like plant viruses maintain different levels of population diversity in a common host. J Virol 74:3130–3134 [View Article][PubMed]
     [Google Scholar]
  49. Schneider W. L., Roossinck M. J. 2001; Genetic diversity in RNA virus quasispecies is controlled by host–virus interactions. J Virol 75:6566–6571 [View Article][PubMed]
     [Google Scholar]
  50. Smith-Tsurkan S. D., Wilke C. O., Novella I. S. 2010; Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types. J Gen Virol 91:1484–1493 [View Article][PubMed]
     [Google Scholar]
  51. Steinhauer D. A., Domingo E., Holland J. J. 1992; Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 122:281–288 [View Article][PubMed]
     [Google Scholar]
  52. Tesh R. B., Modi G. B. 1983; Development of a continuous cell line from the sand fly Lutzomyia longipalpis (Diptera: Psychodidae), and its susceptibility to infection with arboviruses. J Med Entomol 20:199–202[PubMed] [CrossRef]
     [Google Scholar]
  53. Turner P. E., Morales N. M., Alto B. W., Remold S. K. 2010; Role of evolved host breadth in the initial emergence of an RNA virus. Evolution 64:3273–3286 [View Article][PubMed]
     [Google Scholar]
  54. Whitlock M. C. 1992; Temporal fluctuations in demographic parameters and the genetic variance among populations. Evolution 46:608–615 [View Article]
     [Google Scholar]
  55. Whitlock M. C. 1996; The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. Am Nat 148:Suppl.S65–S77 [View Article]
     [Google Scholar]
  56. Wilke C. O., Novella I. S. 2003; Phenotypic mixing and hiding may contribute to memory in viral quasispecies. BMC Microbiol 3:11 [View Article][PubMed]
     [Google Scholar]
  57. Wilke C. O., Reissig D. D., Novella I. S. 2004; Replication at periodically changing multiplicity of infection promotes stable coexistence of competing viral populations. Evolution 58:900–905[PubMed] [CrossRef]
     [Google Scholar]
  58. Zárate S., Novella I. S. 2004; Vesicular stomatitis virus evolution during alternation between persistent infection in insect cells and acute infection in mammalian cells is dominated by the persistence phase. J Virol 78:12236–12242 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.048082-0
Loading
The role of environmental factors on the evolution of phenotypic diversity in vesicular stomatitis virus populations
J. Gen. Virol. 94, 860 (2013); https://doi.org/10.1099/vir.0.048082-0
/content/journal/jgv/10.1099/vir.0.048082-0
/content/journal/jgv/10.1099/vir.0.048082-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error