Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2002 Mar 22;269(1491):591–597. doi: 10.1098/rspb.2001.1902

Mutator dynamics in fluctuating environments.

J M J Travis 1, E R Travis 1
PMCID: PMC1690933  PMID: 11916475

Abstract

Populations with high mutation rates (mutator clones) are being found in increasing numbers of species, and a clear link is being established between the presence of mutator clones and drug resistance. Mutator clones exist despite the fact that in a constant environment most mutations are deleterious, with the spontaneous mutation rate generally held at a low value. This implies that mutator clones have an important role in the adaptation of organisms to changing environments. Our study examines how mutator dynamics vary according to the frequency of environmental fluctuations. Although recent studies have considered a single environmental switch, here we investigate mutator dynamics in a regularly varying environment, seeking to mimic conditions present, for example, under certain drug or pesticide regimes. Our model provides four significant new insights. First, the results demonstrate that mutators are most prevalent under intermediate rates of environmental change. When the environment oscillates more rapidly, mutators are unable to provide sufficient adaptability to keep pace with the frequent changes in selection pressure and, instead, a population of 'environmental generalists' dominates. Second, our findings reveal that mutator dynamics may be complex, exhibiting limit cycles and chaos. Third, we demonstrate that when each beneficial mutation provides a greater gain in fitness, mutators achieve higher densities in more rapidly fluctuating environments. Fourth, we find that mutators of intermediate strength reach higher densities than very weak or strong mutators.

Full Text

The Full Text of this article is available as a PDF (182.5 KB).

Selected References

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

  1. Ayala F. J. Neutralism and selectionism: the molecular clock. Gene. 2000 Dec 30;261(1):27–33. doi: 10.1016/s0378-1119(00)00479-0. [DOI] [PubMed] [Google Scholar]
  2. Drake J. W. A constant rate of spontaneous mutation in DNA-based microbes. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7160–7164. doi: 10.1073/pnas.88.16.7160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Earn D. J., Rohani P., Grenfell B. T. Persistence, chaos and synchrony in ecology and epidemiology. Proc Biol Sci. 1998 Jan 7;265(1390):7–10. doi: 10.1098/rspb.1998.0256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Gillespie J. H. Lineage effects and the index of dispersion of molecular evolution. Mol Biol Evol. 1989 Nov;6(6):636–647. doi: 10.1093/oxfordjournals.molbev.a040576. [DOI] [PubMed] [Google Scholar]
  5. Giraud A., Matic I., Tenaillon O., Clara A., Radman M., Fons M., Taddei F. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science. 2001 Mar 30;291(5513):2606–2608. doi: 10.1126/science.1056421. [DOI] [PubMed] [Google Scholar]
  6. Henry K., Erice A., Tierney C., Balfour H. H., Jr, Fischl M. A., Kmack A., Liou S. H., Kenton A., Hirsch M. S., Phair J. A randomized, controlled, double-blind study comparing the survival benefit of four different reverse transcriptase inhibitor therapies (three-drug, two-drug, and alternating drug) for the treatment of advanced AIDS. AIDS Clinical Trial Group 193A Study Team. J Acquir Immune Defic Syndr Hum Retrovirol. 1998 Dec 1;19(4):339–349. doi: 10.1097/00042560-199812010-00004. [DOI] [PubMed] [Google Scholar]
  7. Ishii K., Matsuda H., Iwasa Y., Sasaki A. Evolutionarily stable mutation rate in a periodically changing environment. Genetics. 1989 Jan;121(1):163–174. doi: 10.1093/genetics/121.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kibota T. T., Lynch M. Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature. 1996 Jun 20;381(6584):694–696. doi: 10.1038/381694a0. [DOI] [PubMed] [Google Scholar]
  9. LeClerc J. E., Li B., Payne W. L., Cebula T. A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science. 1996 Nov 15;274(5290):1208–1211. doi: 10.1126/science.274.5290.1208. [DOI] [PubMed] [Google Scholar]
  10. Leigh E. G., Jr The evolution of mutation rates. Genetics. 1973 Apr;73(Suppl):1–18. [PubMed] [Google Scholar]
  11. Mansky L. M., Cunningham K. S. Virus mutators and antimutators: roles in evolution, pathogenesis and emergence. Trends Genet. 2000 Nov;16(11):512–517. doi: 10.1016/s0168-9525(00)02125-9. [DOI] [PubMed] [Google Scholar]
  12. Mao E. F., Lane L., Lee J., Miller J. H. Proliferation of mutators in A cell population. J Bacteriol. 1997 Jan;179(2):417–422. doi: 10.1128/jb.179.2.417-422.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Matic I., Radman M., Taddei F., Picard B., Doit C., Bingen E., Denamur E., Elion J. Highly variable mutation rates in commensal and pathogenic Escherichia coli. Science. 1997 Sep 19;277(5333):1833–1834. doi: 10.1126/science.277.5333.1833. [DOI] [PubMed] [Google Scholar]
  14. Ninio J. Transient mutators: a semiquantitative analysis of the influence of translation and transcription errors on mutation rates. Genetics. 1991 Nov;129(3):957–962. doi: 10.1093/genetics/129.3.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Oliver A., Cantón R., Campo P., Baquero F., Blázquez J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science. 2000 May 19;288(5469):1251–1254. doi: 10.1126/science.288.5469.1251. [DOI] [PubMed] [Google Scholar]
  16. Ota T., Kimura M. On the constancy of the evolutionary rate of cistrons. J Mol Evol. 1971;1(1):18–25. doi: 10.1007/BF01659391. [DOI] [PubMed] [Google Scholar]
  17. Sniegowski P. D., Gerrish P. J., Johnson T., Shaver A. The evolution of mutation rates: separating causes from consequences. Bioessays. 2000 Dec;22(12):1057–1066. doi: 10.1002/1521-1878(200012)22:12<1057::AID-BIES3>3.0.CO;2-W. [DOI] [PubMed] [Google Scholar]
  18. Sniegowski P. D., Gerrish P. J., Lenski R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature. 1997 Jun 12;387(6634):703–705. doi: 10.1038/42701. [DOI] [PubMed] [Google Scholar]
  19. Taddei F., Radman M., Maynard-Smith J., Toupance B., Gouyon P. H., Godelle B. Role of mutator alleles in adaptive evolution. Nature. 1997 Jun 12;387(6634):700–702. doi: 10.1038/42696. [DOI] [PubMed] [Google Scholar]
  20. Tenaillon O., Toupance B., Le Nagard H., Taddei F., Godelle B. Mutators, population size, adaptive landscape and the adaptation of asexual populations of bacteria. Genetics. 1999 Jun;152(2):485–493. doi: 10.1093/genetics/152.2.485. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES