1887

Journal of General Virology header logo

Volume 91, Issue 6

Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types Free

Abstract

Host radiation refers to the ability of parasites to adapt to new environments and expand or change their niches. Adaptation to one specific environment may involve a loss in adaptation to a second environment. Thus, fitness costs may impose limits to niche expansion and constitute the cost of specialization. Several reports have addressed the cost of host radiation in vesicular stomatitis virus (VSV), but in some cases the experimental setup may have resulted in the overestimation of fitness costs. To clarify this issue, experiments were carried out in which a reference strain of VSV was allowed to adapt to HeLa, MDCK and BHK-21 cells, and to a regime of alternation between HeLa and Madin–Darby canine kidney (MDCK) cells. Measurement of viral fitness on each cell type showed that most virus populations behaved as generalists, and increased in fitness in all environments. Tradeoffs, where a fitness increase in one environment led to a fitness decrease in another environment, were rare. These results highlight the importance of using appropriate methods to measure fitness in evolved virus populations, and provide further support to a model of evolutionary dynamics in which costs due to incongruent landscapes provided by different environments are more common than tradeoffs.

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

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.017855-0
2010-06-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/6/1484.html?itemId=/content/journal/jgv/10.1099/vir.0.017855-0&mimeType=html&fmt=ahah

References

  1. Bolnick, D. I.(2001). Intraspecific competition favours niche width expansion in Drosophila melanogaster. Nature 410, 463–466.[CrossRef] [Google Scholar]
  2. Buckling, A., Wills, M. A. & Colegrave, N.(2003). Adaptation limits diversification of experimental bacterial populations. Science 302, 2107–2109.[CrossRef] [Google Scholar]
  3. Chen, W. J., Wu, H. R. & Chiou, S. S.(2003). E/NS1 modifications of dengue 2 virus after serial passages in mammalian and/or mosquito cells. Intervirology 46, 289–295.[CrossRef] [Google Scholar]
  4. Ciota, A. T., Lovelace, A. O., Ngo, K. A., Le, A. N., Maffei, J. G., Franke, M. A., Payne, A. F., Jones, S. A., Kauffman, E. B. & Kramer, L. D.(2007). Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology 357, 165–174.[CrossRef] [Google Scholar]
  5. Clarke, D. K., Duarte, E. A., Moya, A., Elena, S. F., Domingo, E. & Holland, J.(1993). Genetic bottlenecks and population passages cause profound fitness differences in RNA viruses. J Virol 67, 222–228. [Google Scholar]
  6. Clarke, D. K., Duarte, E. A., Elena, S. F., Moya, A., Domingo, E. & Holland, J.(1994). The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci U S A 91, 4821–4824.[CrossRef] [Google Scholar]
  7. Coffey, L. L., Vasilakis, N., Brault, A. C., Powers, A. M., Tripet, F. & Weaver, S. C.(2008). Arbovirus evolution in vivo is constrained by host alternation. Proc Natl Acad Sci U S A 105, 6970–6975.[CrossRef] [Google Scholar]
  8. Cooper, L. A. & Scott, T. W.(2001). Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157, 1403–1412. [Google Scholar]
  9. Cuevas, J. M., Elena, S. F. & Moya, A.(2002). Molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics 162, 533–542. [Google Scholar]
  10. Domingo, E., Biebricher, C. K., Eigen, M. & Holland, J. J.(2001).Quasispecies and RNA Virus Evolution: Principles and Consequences. Georgetown, TX: Lands Bioscience.
  11. Elena, S. F. & Lenski, R. E.(2003). Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4, 457–469. [Google Scholar]
  12. Elena, S. F., Miralles, R. & Moya, A.(1997). Frequency-dependent selection in a mammalian RNA virus. Evolution 51, 984–987.[CrossRef] [Google Scholar]
  13. Feuer, R., Boone, J. D., Netski, D., Morzunov, S. P. & St Jeor, S. C.(1999). Temporal and spatial analysis of Sin Nombre virus quasispecies in naturally infected rodents. J Virol 73, 9544–9554. [Google Scholar]
  14. Fry, J. D.(1996). The evolution of host specialization: are tradeoffs overrated? Am Nat 148, S84–S107.[CrossRef] [Google Scholar]
  15. Greene, I. P., Wang, E. Y., Deardorff, E. R., Milleron, R., Domingo, E. & Weaver, S. C.(2005). Effect of alternating passage on adaptation of Sindbis virus to vertebrate and invertebrate cells. J Virol 79, 14253–14260.[CrossRef] [Google Scholar]
  16. Holland, J. J., Delatorre, 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. [Google Scholar]
  17. Hothorn, T., Bretz, F. & Westfall, P.(2008). Simultaneous inference in general parametric models. Biom J 50, 346–363.[CrossRef] [Google Scholar]
  18. Kassen, R.(2002). The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15, 173–190.[CrossRef] [Google Scholar]
  19. Kassen, R. & Rainey, P. B.(2004). The ecology and genetics of microbial diversity. Annu Rev Microbiol 58, 207–231.[CrossRef] [Google Scholar]
  20. MacLean, R. C., Bell, G. & Rainey, P. B.(2004). The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proc Natl Acad Sci U S A 101, 8072–8077.[CrossRef] [Google Scholar]
  21. McKinnon, J. S. & Rundle, H. D.(2002). Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17, 480–488.[CrossRef] [Google Scholar]
  22. Novella, I. S.(2003). Contributions of vesicular stomatitis virus to the understanding of RNA virus evolution. Curr Opin Microbiol 6, 399–405.[CrossRef] [Google Scholar]
  23. Novella, I. S.(2004). Negative effect of genetic bottlenecks on the adaptability of vesicular stomatitis virus. J Mol Biol 336, 61–67.[CrossRef] [Google Scholar]
  24. Novella, I. S., Clarke, D. K., Quer, J., Duarte, E. A., Lee, C. H., Weaver, S. C., Elena, S. F., Moya, A., Domingo, E. & Holland, J. J.(1995a). Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandfly cells. J Virol 69, 6805–6809. [Google Scholar]
  25. Novella, I. S., Duarte, E. A., Elena, S. F., Moya, A., Domingo, E. & Holland, J. J.(1995b). Exponential increases of RNA virus fitness during large population transmissions. Proc Natl Acad Sci U S A 92, 5841–5844.[CrossRef] [Google Scholar]
  26. Novella, I. S., Elena, S. F., Moya, A., Domingo, E. & Holland, J. J.(1995c). Size of genetic bottlenecks leading to virus fitness loss is determined by mean initial population fitness. J Virol 69, 2869–2872. [Google Scholar]
  27. Novella, I. S., Hershey, C. L., Escarmis, C., Domingo, E. & Holland, J. J.(1999). Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287, 459–465.[CrossRef] [Google Scholar]
  28. Novella, I. S., Zarate, S., Metzgar, D. & Ebendick-Corpus, B. E.(2004). Positive selection of synonymous mutations in vesicular stomatitis virus. J Mol Biol 342, 1415–1421.[CrossRef] [Google Scholar]
  29. O'Keefe, K. J., Morales, N. M., Ernstberger, H., Benoit, G. & Turner, P. E.(2006). Laboratory-dependent bacterial ecology: a cautionary tale. Appl Environ Microbiol 72, 3032–3035.[CrossRef] [Google Scholar]
  30. Quer, J., Huerta, R., Novella, I. S., Tsimring, L., Domingo, E. & Holland, J. J.(1996). Reproducible nonlinear population dynamics and critical points during replicative competitions of RNA virus quasispecies. J Mol Biol 264, 465–471.[CrossRef] [Google Scholar]
  31. Rainey, P. B. & Travisano, M.(1998). Adaptive radiation in a heterogeneous environment. Nature 394, 69–72.[CrossRef] [Google Scholar]
  32. Remold, S. K., Rambaut, A. & Turner, P. E.(2008). Evolutionary genomics of host adaptation in vesicular stomatitis virus. Mol Biol Evol 25, 1138–1147.[CrossRef] [Google Scholar]
  33. Sander, P., Springer, B., Prammananan, T., Sturmfels, A., Kappler, M., Pletschette, M. & Bottger, E. C.(2002). Fitness cost of chromosomal drug resistance-conferring mutations. Antimicrob Agents Chemother 46, 1204–1211.[CrossRef] [Google Scholar]
  34. Scheipl, F., Greven, S. & Kuchenhoff, H.(2008). Size and power of tests for a zero random effect variance or polynomial regression in additive and linear mixed models. Comput Stat Data Anal 52, 3283–3299.[CrossRef] [Google Scholar]
  35. Schliewen, U., Rassmann, K., Markmann, M., Markert, J., Kocher, T. & Tautz, D.(2001). Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon. Mol Ecol 10, 1471–1488.[CrossRef] [Google Scholar]
  36. Turner, P. E. & Elena, S. F.(2000). Cost of host radiation in an RNA virus. Genetics 156, 1465–1470. [Google Scholar]
  37. Weaver, S. C., Brault, A. C., Kang, W. L. & Holland, J. J.(1999). Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73, 4316–4326. [Google Scholar]
  38. Weber, K. E.(1996). Large genetic change at small fitness cost in large populations of Drosophila melanogaster selected for wind tunnel flight: rethinking fitness surfaces. Genetics 144, 205–213. [Google Scholar]
  39. Whitlock, M. C.(1992). Temporal fluctuations in demographic parameters and the genetic variance among populations. Evolution 46, 608–615.[CrossRef] [Google Scholar]
  40. 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.[CrossRef] [Google Scholar]
  41. Zarate, 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.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.017855-0
Loading
Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types
J. Gen. Virol. 91, 1484 (2010); https://doi.org/10.1099/vir.0.017855-0
/content/journal/jgv/10.1099/vir.0.017855-0
/content/journal/jgv/10.1099/vir.0.017855-0
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