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Microbial genetics

Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation

Key Points

  • Microorganisms are well-suited for experimental studies of evolution owing to their rapid generations and large populations, as well as the wealth of molecular and genomic data that are available for many species.

  • Genetic adaptation is especially rapid when microbial populations are introduced into new environments, although they may continue to improve indefinitely, even under a constant regime.

  • Genetic comparisons of ancestral and experimentally evolved microbes provide some striking examples of parallel molecular evolution in replicate populations, including examples of adaptive mutations in genes that encode important global regulators.

  • Genetic adaptation to one environment is often, although not always, associated with fitness loss in other environments, and antagonistic pleiotropy often seems to be responsible for these tradeoffs.

  • Asexual populations that are rapidly adapting to new or changing environments provide opportunities for hypermutable genotypes to hitchhike with the beneficial mutations that they may generate, although the emergence of mutators does not always greatly accelerate adaptive evolution.

  • Very small populations, including those that experience repeated bottlenecks, do not improve over time, but instead suffer genetic decay because the random processes of mutation and drift overwhelm the capacity of selection to retain well-adapted genotypes.

Abstract

Microorganisms have been mutating and evolving on Earth for billions of years. Now, a field of research has developed around the idea of using microorganisms to study evolution in action. Controlled and replicated experiments are using viruses, bacteria and yeast to investigate how their genomes and phenotypic properties evolve over hundreds and even thousands of generations. Here, we examine the dynamics of evolutionary adaptation, the genetic bases of adaptation, tradeoffs and the environmental specificity of adaptation, the origin and evolutionary consequences of mutators, and the process of drift decay in very small populations.

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Figure 1: Fitness landscapes and evolutionary dynamics.
Figure 2: Tradeoffs and specificity of adaptation.
Figure 3: Role of mutators in generating variation.
Figure 4: Population bottlenecks and accumulation of deleterious mutations.

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References

  1. Zuckerkandl, E. & Pauling, L. in Evolving Genes and Proteins (eds Bryson, V. & Vogel, H. J.) 97–166 (Academic Press, New York, 1965).

    Book  Google Scholar 

  2. Harvey, P. H. & Pagel, M. D. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, Oxford, UK, 1991).

    Google Scholar 

  3. Darwin, C. On the Origin of Species by Means of Natural Selection (Murray, London, 1859).

    Google Scholar 

  4. Chadwick, D. J. & Goode, J. (eds) Antibiotic Resistance: Origins, Evolution, Selection and Spread (Wiley, Chichester, UK, 1997).

    Google Scholar 

  5. Grant, P. R. Ecology and Evolution of Darwin's Finches (Princeton Univ. Press, Princeton, 1999).

    Google Scholar 

  6. Atwood, K. C., Schneider, L. K. & Ryan, F. J. Periodic selection in Escherichia coli. Proc. Natl Acad. Sci. USA 37, 146–155 (1951).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ryan, F. J. Evolution observed. Sci. Am. 189, 78–82 (1953).

    Article  Google Scholar 

  8. Hairston, N. G. Evolution under interspecific competition: field experiments on terrestrial salamanders. Evolution 34, 409–420 (1980).

    Article  PubMed  Google Scholar 

  9. Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Levin, B. R. & Bergstrom, C. T. Bacteria are different: observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes. Proc. Natl Acad. Sci. USA 97, 6981–6985 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bell, G. C. Selection (Chapman & Hall, New York, 1997).

    Book  Google Scholar 

  12. Holland, J. J., de la Torre, J. C., Clarke, D. K. & Duarte, E. A. Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J. Virol. 65, 2960–2967 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).

    Article  Google Scholar 

  14. Hall, B. G. in Evolution of Genes and Proteins (eds Nei, M. & Koehn, R. K.) 234–257 (Sinauer, Sunderland, Massachusetts, 1983).

    Google Scholar 

  15. Mortlock, R. R. (ed.) Microorganisms as Model Systems for Studying Evolution (Plenum, New York, 1984).

    Google Scholar 

  16. Sniegowski, P. D. & R. E. Lenski . Mutation and adaptation: the directed mutation controversy in evolutionary perspective. Ann. Rev. Ecol. Syst. 26, 553–578 (1995).

    Article  Google Scholar 

  17. Roth J. R. et al. Regulating general mutation rates: examination of the hypermutable state model for Cairnsian adaptive mutation. Genetics 163, 1483–1496 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dykhuizen, D. E. & Dean, A. M. Enzyme activity and fitness: evolution in solution. Trends Ecol. Evol. 5, 257–262 (1990).

    Article  CAS  PubMed  Google Scholar 

  19. Dykhuizen, D. E. in Population Genetics of Bacteria (eds Baumberg, S., Young, J. P. W., Saunders, S. R. & Wellington, E. M. H.) 161–173 (Cambridge Univ. Press, Cambridge, UK, 1995).

    Google Scholar 

  20. Dykhuizen, D. E. Experimental studies of natural selection in bacteria. Ann. Rev. Ecol. Syst. 21, 373–398 (1990).

    Article  Google Scholar 

  21. Fisher, R. A. The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, UK, 1930).

    Book  Google Scholar 

  22. Orr, H. A. The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52, 935–949 (1998).

    Article  PubMed  Google Scholar 

  23. Gould, S. J. Wonderful Life: the Burgess Shale and the Nature of History (Norton, New York, 1989).

    Google Scholar 

  24. Conway Morris, S. The Crucible of Creation (Oxford Univ. Press, Oxford, UK, 1998).

    Google Scholar 

  25. Lenski, R. E. & Travisano, M. Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Proc. Natl Acad. Sci. USA 91, 6808–6814 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cooper, V. S. & Lenski, R. E. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407, 736–739 (2000). This article shows the dynamics of adaptation to glucose over 20,000 generations, along with resource specialization that is caused primarily by antagonistic pleiotropy.

    Article  CAS  PubMed  Google Scholar 

  27. Novella, I. S. et al. Exponential increases of RNA virus fitness during repeated transmission. Proc. Natl Acad. Sci. USA 92, 5841–5844 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bull, J. J. et al. Exceptional convergent evolution in a virus. Genetics 147, 1497–1507 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Elena, S. F. et al. Evolutionary dynamics of fitness recovery from the debilitating effects of Muller's ratchet. Evolution 52, 309–314 (1998).

    Article  PubMed  Google Scholar 

  30. De Visser, J. A. G. M. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. XI. Rejection of non-transitive interactions as cause of declining rate of adaptation. BMC Evol. Biol. 2, 19 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Burch, C. L. & Chao, L. Evolution by small steps and rugged landscapes in the RNA virus φ6. Genetics 151, 921–927 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Elena, S. F., Cooper, V. S. & Lenski, R. E. Punctuated evolution caused by selection of rare beneficial mutations. Science 272, 1802–1804 (1996).

    Article  CAS  PubMed  Google Scholar 

  33. Gerrish, P. J. & Lenski, R. E. The fate of competing beneficial mutations in an asexual population. Genetica 102/103, 127–144 (1998).

    Article  Google Scholar 

  34. Imhof, M. & Schlötterer, C. Fitness effects of advantageous mutations in evolving Escherichia coli populations. Proc. Natl Acad. Sci. USA 98, 1113–1117 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Rozen, D. E., De Visser, J. A. G. M. & Gerrish, P. J. Fitness effects of fixed beneficial mutations in microbial populations. Curr. Biol. 12, 1040–1045 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. De Visser, J. A. G. M., Zeyl, C. W., Gerrish, P. J., Blanchard, J. L. & Lenski, R. E. Diminishing returns from mutation supply rate in asexual populations. Science 283, 404–406 (1999).

    Article  CAS  Google Scholar 

  37. Papadopoulos, D. et al. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl Acad. Sci. USA 96, 3807–3812 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Shaver, A. C. et al. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162, 557–566 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Miralles, R., Gerrish, P. J., Moya, A. & Elena, S. F. Clonal interference and the evolution of RNA viruses. Science 285, 1745–1747 (1999).

    Article  CAS  PubMed  Google Scholar 

  40. Miralles, R., Moya, A. & Elena, S. F. Diminishing returns of population size in the rate of RNA virus adaptation. J. Virol. 74, 3566–3571 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Cuevas, J. M., Elena, S. F. & Moya, A. Molecular basis of adaptive convergence in experimental populations of RNA viruses. Genetics 162, 533–542 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Korona, R., Nakatsu, C. H., Forney, L. J. & Lenski, R. E. Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc. Natl Acad. Sci. USA 91, 9037–9041 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Goho, S. & Bell, G. The ecology and genetics of fitness in Chlamydomonas. IX. The rate of accumulation of variation of fitness under selection. Evolution 54, 416–424 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Vasi, F., Travisano, M. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am. Nat. 144, 432–456 (1994).

    Article  Google Scholar 

  45. Lenski, R. E. & Mongold, J. A. in Scaling in Biology (eds Brown, J. H. & West, G. B.) 221–235 (Oxford Univ. Press, Oxford, UK, 2000).

    Google Scholar 

  46. Riley, M. S., Cooper, V. S., Lenski, R. E., Forney, L. J. & Marsh T. L. Rapid phenotypic change and diversification of a soil bacterium during 1000 generations of experimental evolution. Microbiology 147, 995–1006 (2001).

    Article  CAS  PubMed  Google Scholar 

  47. Bennett, A. F. & Lenski, R. E. Evolutionary adaptation to temperature. II. Thermal niches of experimental lines of Escherichia coli. Evolution 47, 1–12 (1993).

    Article  PubMed  Google Scholar 

  48. Travisano, M. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143, 15–26 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Cooper, V. S. Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. BMC Evol. Biol. 2, 12 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Travisano, M., Mongold, J. A., Bennett, A. F. & Lenski, R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

    Article  CAS  PubMed  Google Scholar 

  51. Burch, C. L. & Chao, L. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406, 625–628 (2000).

    Article  CAS  PubMed  Google Scholar 

  52. Drake, J. W. & Holland, J. J. Mutation rates among RNA viruses. Proc. Natl Acad. Sci. USA 96, 13910–13913 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Cunningham, C. W. et al. Parallel molecular evolution of deletions and nonsense mutations in bacteriophage T7. Mol. Biol. Evol. 14, 113–116 (1997).

    Article  CAS  PubMed  Google Scholar 

  54. Wichman, H. A., Badgett, M. R., Scott, L. A., Boulianne, C. M. & Bull, J. J. Different trajectories of parallel evolution during viral adaptation. Science 285, 422–424 (1999).

    Article  CAS  PubMed  Google Scholar 

  55. Wichman, H. A., Yarber, C. D., Scott, L. A. & Bull, J. J. Experimental evolution recapitulates natural evolution. Phil. Trans. R. Soc. Lond. B 355, 1–8 (2000). A remarkable study of parallel and convergent molecular evolution that is based on the whole-genome sequencing of viruses.

    Article  Google Scholar 

  56. Bull, J. J., Badgett, M. R. & Wichman, H. A. Big-benefit mutations in bacteriophage inhibited with heat. Mol. Biol. Evol. 17, 942–950 (2000).

    Article  CAS  PubMed  Google Scholar 

  57. Lenski, R. E., Winkworth, C. L. & Riley, M. A. Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J. Mol. Evol. 56, 498–508 (2003).

    Article  CAS  PubMed  Google Scholar 

  58. Cooper, T. F., Rozen, D. E. & Lenski, R. E. Parallel changes in gene expression after 20,000 generations of evolution in E. coli. Proc. Natl Acad. Sci. USA 100, 1072–1077 (2003). Whole-genome arrays show parallel changes in gene expression, which led to the discovery of beneficial mutations in an important regulatory gene.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Zhang, E. & Ferenci, T. OmpF changes and the complexity of Escherichia coli adaptation to prolonged lactose limitation. FEMS Microbiol. Lett. 176, 395–401 (1999).

    Article  CAS  PubMed  Google Scholar 

  60. Notley-McRobb, L. & Ferenci, T. Adaptive mgl-regulatory mutations and genetic diversity evolving in glucose-limited Escherichia coli populations. Env. Microbiol. 1, 33–43 (1999).

    Article  CAS  Google Scholar 

  61. Notley-McRobb, L. & Ferenci, T. The generation of multiple co-existing mal-regulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Env. Microbiol. 1, 45–52 (1999). Candidate loci that are involved in glucose transport show diverse mutational pathways to enhanced fitness in chemostat-adapted populations.

    Article  CAS  Google Scholar 

  62. Notley-McRobb, L. & Ferenci, T. Experimental analysis of molecular events during mutational periodic selections in bacterial evolution. Genetics 156, 1493–1501 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Rosenzweig, R. F., Sharp, R. R., Treves, D. S. & Adams, J. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137, 903–917 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Treves, D. S., Manning, S. & Adams, J. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol. Biol. Evol. 15, 789–797 (1998).

    Article  CAS  PubMed  Google Scholar 

  65. Mikkola, R. & Kurland, C. G. Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol. Biol. Evol. 9, 394–402 (1992).

    CAS  PubMed  Google Scholar 

  66. Zambrano, M. M., Siegele, D. A., Almiron, M., Tormo, A. & Kolter, R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259, 1757–1760 (1993). Selection under starvation conditions favours mutations in a σ-factor.

    Article  CAS  PubMed  Google Scholar 

  67. Finkel, S. E. & Kolter, R. Evolution of microbial diversity during prolonged starvation. Proc. Natl Acad. Sci. USA 96, 4023–4027 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Zinser, E. R. & Kolter, R. Prolonged stationary-phase incubation selects for lrp mutations in Escherichia coli K-12. J. Bacteriol. 182, 4361–4365 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Kurlandzka, A., Rosenzweig, R. F. & Adams, J. Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. Mol. Biol. Evol. 8, 261–281 (1991).

    CAS  PubMed  Google Scholar 

  70. Ferea, T. L., Botstein, D., Brown, P. O. & Rosenzweig, R. F. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc. Natl Acad. Sci. USA 96, 9721–9726 (1999). The first application of gene-expression arrays to experimental evolution, showing parallel changes in central metabolism in three yeast lines.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Riehle, M. R., Bennett, A. F., Lenski, R. E. & Long, A. D. Evolutionary changes in heat-inducible gene expression in lines of Escherichia coli adapted to high temperature. Physiol. Genomics (in the press).

  72. Cowen, L. E. et al. Evolution of drug resistance in experimental populations of Candida albicans. J. Bacteriol. 182, 1515–1522 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Cowen, L. E. et al. Population genomics of drug resistance in Candida albicans. Proc. Natl Acad. Sci. USA 99, 9284–9289 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. King, M. -C. & Wilson, A. C. Evolution at two levels in humans and chimpanzees. Science 188, 107–116 (1975).

    Article  CAS  PubMed  Google Scholar 

  75. Wilke, C. M., Maimer, E. & Adams, J. The population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae. Genetica 86, 155–173 (1992).

    Article  CAS  PubMed  Google Scholar 

  76. Dunham, M. J. et al. Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 99, 16144–16149 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Naas, T., Blot, M., Fitch, W. M. & Arber, W. Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. Mol. Biol. Evol. 12, 198–207 (1995). Shows the usefulness of transposable elements for discovering cryptic genetic changes, even in cultures that are 'stored' at room temperature.

    CAS  PubMed  Google Scholar 

  78. Schneider, D., Duperchy, E., Coursange, E., Lenski, R. E. & Blot, M. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156, 477–488 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Cooper, V. S., Schneider, D., Blot, M. & Lenski, R. E. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J. Bacteriol. 183, 2834–2841 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Riehle, M. M., Bennett, A. F. & Long, A. D. Genetic architecture of thermal adaptation in Escherichia coli. Proc. Natl Acad. Sci. USA 98, 525–530 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, UK, 2000).

    Google Scholar 

  82. Levins, R. Evolution in Changing Environments (Princeton Univ. Press, Princeton, 1968).

    Book  Google Scholar 

  83. Chao, L., Levin, B. R. & Stewart, F. M. A complex community in a simple habitat: an experimental study with bacteria and phage. Ecology 58, 369–378 (1977).

    Article  Google Scholar 

  84. Lenski, R. E. & Levin, B. R. Constraints on the coevolution of bacteria and virulent phage: a model, some experiments, and predictions for natural communities. Am. Nat. 125, 585–602 (1985).

    Article  Google Scholar 

  85. Lenski, R. E. Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution 42, 425–432 (1988).

    PubMed  Google Scholar 

  86. Funchain, P., Yeung, A. Stewart, J. L., Lin, R., Slupsa, M. M. & Miller, J. H. The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154, 959–970 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Giraud, A. et al. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291, 2606–2608 (2001). Pioneering work that shows that rigorous evolution experiments can be carried out in animal hosts, and also indicates important effects of mutator genotypes.

    Article  CAS  PubMed  Google Scholar 

  88. Mongold, J. A., Bennett, A. F. & Lenski, R. E. Evolutionary adaptation to temperature. IV. Adaptation of Escherichia coli at a niche boundary. Evolution 50, 35–43 (1996).

    Article  PubMed  Google Scholar 

  89. Travisano, M., Vasi, F. & Lenski, R. E. Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49, 189–200 (1995).

    PubMed  Google Scholar 

  90. Travisano, M. Long-term experimental evolution in Escherichia coli. VI. Environmental constraints on adaptation and divergence. Genetics 146, 471–479 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Dykhuizen, D. & Hartl, D. Evolution of competitive ability in Escherichia coli. Evolution 35, 581–594 (1981).

    Article  PubMed  Google Scholar 

  92. Velicer, G. J. & Lenski, R. E. Evolutionary tradeoffs under conditions of resource abundance and scarcity: experiments with bacteria. Ecology 80, 1168–1179 (1999).

    Article  Google Scholar 

  93. Reboud, X. & Bell, G. Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78, 507–514 (1997).

    Article  Google Scholar 

  94. Novella, I. S. et al. Extreme fitness differences in mammalian and insect hosts after continuous replication of vesicular stomatitis virus in sandly cells. J. Virol. 69, 6805–6809 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Crill, W. D., Wichman, H. A. & Bull, J. J. Evolutionary reversals during viral adaptation to alternating hosts. Genetics 154, 27–37 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Turner, P. E. & Elena, S. F. Cost of host radiation in an RNA virus. Genetics 156, 1465–1670 (2000). A study, using viruses, that shows the tradeoffs on the original host during adaptation to new hosts, as well as selection for generalists in fluctuating environments.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Cooper, L. A. & Scott, T. W. Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157, 1403–1412 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Weaver, W. C., Brault, A. C., Kang, W. & Holland, J. J. Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J. Virol. 73, 4316–4326 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Novella, I. S., Hershey, C. L., Escarmís, C., Domingo, E. & Holland, J. J. Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J. Mol. Biol. 287, 459–465 (1999).

    Article  CAS  PubMed  Google Scholar 

  100. Ebert, D. Experimental evolution of parasites. Science 282, 1432–1435 (1998).

    Article  CAS  PubMed  Google Scholar 

  101. Friedberg, E. C., Walker, G. C. & Siede, W. DNA Repair and Mutagenesis (ASM, Washington, 1995).

    Google Scholar 

  102. Chao, L., Vargas, C., Spear, B. B. & Cox, E. C. Transposable elements as mutator genes in evolution. Nature 303, 633–635 (1983).

    Article  CAS  PubMed  Google Scholar 

  103. Taddei, F. et al. Role of mutator alleles in adaptive evolution. Nature 387, 700–702 (1997). A theoretical model that shows the complex dynamics and effects of alleles that cause increased mutation rates in asexual populations.

    Article  CAS  PubMed  Google Scholar 

  104. LeClerc, J. E., Li, B., Payne, W. L. & Cebula, T. A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274, 1208–1211 (1996).

    Article  CAS  PubMed  Google Scholar 

  105. Oliver, A., Canton, R., Campo, P., Baquero, F. & Blázquez, J. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288, 1251–1253 (2000).

    Article  CAS  PubMed  Google Scholar 

  106. Mao, E. F., Lane, L. Lee, J. & Miller, J. H. Proliferation of mutators in a cell population. J. Bacteriol. 179, 417–422 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of E. coli. Nature 387, 703–705 (1997). This article documents the spontaneous evolution of repair-defective mutators during long-term adaptation to a new environment.

    Article  CAS  PubMed  Google Scholar 

  108. Notley-McRobb, L., Seeto, S. & Ferenci, T. F. Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 162, 1055–1062 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Chao, L. & Cox, E. C. Competition between high and low mutating strains of Escherichia coli. Evolution 37, 125–134 (1983). An elegant experiment showing how the fate of a mutator allele depends, in a stochastic manner, on its abundance in a population.

    Article  PubMed  Google Scholar 

  110. Lenski, R. E. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium, Escherichia coli. Plant Breed. Rev. (in the press).

  111. Muller, H. J. The relation of recombination to mutational advance. Mut. Res. 1, 2–9 (1964).

    Article  Google Scholar 

  112. Haigh, J. The accumulation of deleterious genes in a population: Muller's ratchet. Theor. Pop. Biol. 14, 251–267 (1978).

    Article  CAS  Google Scholar 

  113. Bateman, A. J. The viability of near-normal irradiated chromosomes. Int. J. Radiat. Biol. 1, 170–180 (1959).

    Google Scholar 

  114. Keightley, P. D. Inference of genome-wide mutation rates and distribution of mutation effects for fitness traits: a simulation study. Genetics 150, 1283–1293 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Mukai, T. The genetic structure of natural populations of Drosophila melanogaster. VII. Synergistic interaction of spontaneous mutant polygenes controlling viability. Genetics 61, 749–761 (1969).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Chao, L. Evolution of sex in RNA viruses. J. Theor. Biol. 133, 99–112 (1988).

    Article  CAS  PubMed  Google Scholar 

  117. Kondrashov, A. S. Deleterious mutations and the evolution of sexual reproduction. Nature 336, 435–440 (1988).

    Article  CAS  PubMed  Google Scholar 

  118. Kondrashov, A. S. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84, 372–387 (1993).

    Article  CAS  PubMed  Google Scholar 

  119. Lynch, M. & Gabriel, W. Mutation load and the survival of small populations. Evolution 44, 1725–1737 (1990).

    Article  PubMed  Google Scholar 

  120. Moran, N. A. Accelerated evolution and Muller's ratchet in endosymbiotic bacteria. Proc. Natl Acad. Sci. USA 93, 2873–2878 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Zeyl, C., Mizesko, M. & De Visser, J. A. G. M. Mutational meltdown in laboratory yeast populations. Evolution 55, 909–917 (2001).

    Article  CAS  PubMed  Google Scholar 

  122. Chao, L. Fitness of RNA virus decreased by Muller's ratchet. Nature 348, 454–455 (1990). An early study that shows the rapid decline in fitness of populations propagated through severe bottlenecks.

    Article  CAS  PubMed  Google Scholar 

  123. Duarte, E. A., Clarke, D. K., Moya, A., Domingo, E. & Holland, J. J. Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet. Proc. Natl Acad. Sci. USA 89, 6015–6019 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Escarmís, C. et al. Genetic lesions associated with Muller's ratchet in a RNA virus. J. Mol. Biol. 264, 255–267 (1996).

    Article  PubMed  Google Scholar 

  125. Elena, S. F. & Moya, A. Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus. J. Evol. Biol. 12, 1078–1088 (1999).

    Article  Google Scholar 

  126. de la Peña, M., Elena, S. F. & Moya, A. Effect of deleterious mutation-accumulation on the fitness of RNA bacteriophage MS2. Evolution 54, 686–691 (2000).

    Article  PubMed  Google Scholar 

  127. Yuste, E., Sánchez-Palomino, S., Casado, C., Domingo, E. & López-Galíndez, C. Drastic fitness loss in human immunodeficiency virus type 1 upon serial bottleneck events. J. Virol. 73, 2745–2751 (2000).

    Article  Google Scholar 

  128. Kibota, T. T. & Lynch, M. Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature 381, 694–696 (1996).

    Article  CAS  PubMed  Google Scholar 

  129. Fares, M. A., Ruiz–González, M. X., Moya, A., Elena, S. F. & Barrio, E. Endosymbiotic bacteria: GroEL buffers against deleterious mutations. Nature 417, 398 (2002).

    Article  CAS  PubMed  Google Scholar 

  130. Wloch, D. M., Szafraniec, K., Borts, R. H. & Korona, R. Direct estimate of the mutation rate and the distribution of fitness effects in the yeast Saccharomyces cerevisiae. Genetics 159, 441–452 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Zeyl, C. & De Visser, J. A. G. M. Estimates of the rate and distribution of fitness effects of spontaneous mutation in Saccharomyces cerevisiae. Genetics 157, 53–61 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Wilke, C. O, Wang, J., Ofria, C., Lenski, R. E. & Adami, C. Evolution of digital organisms at high mutation rate leads to survival of the flattest. Nature 412, 331–333 (2001).

    Article  CAS  PubMed  Google Scholar 

  133. Moore, F. B.-G., Rozen, D. E. & Lenski, R. E. Pervasive compensatory adaptation in Escherichia coli. Proc. R. Soc. Lond. B 267, 515–522 (2000).

    Article  CAS  Google Scholar 

  134. Endy, D., You, L. C., Yin, J. & Molineux, I. J. Computation, prediction, and experimental tests of fitness for bacteriophage T7 mutants with permuted genomes. Proc. Natl Acad. Sci. USA 97, 5375–5380 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. You, L. C. & Yin, J. Dependence of epistasis on environment and mutation severity as revealed by in silico mutagenesis of phage T7. Genetics 160, 1273–1281 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  136. Ibarra, R. U., Edwards, J. S. & Palsson, B. O. Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 420, 186–189 (2002).

    Article  CAS  PubMed  Google Scholar 

  137. Lenski, R. E., Ofria, C., Pennock, R. T. & Adami, C. The evolutionary origin of complex features. Nature 423, 139–144 (2003).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank the reviewers for comments, and N. Hajela for the photographs used in Box 2. S.F.E. is supported at present by the Spanish Consejo Superior de Investigaciones Científicas. R.E.L. is funded by the National Science Foundation and the National Aeronautics and Space Administration.

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DATABASES

BioCyc

acs

GroEL

OmpF

ompF

rpoS

spoT

FURTHER INFORMATION

Adam K. Chippindale's website

E.coli Long-term Experimental Evolution Project Site

Glossary

FITNESS

The average reproductive success of a genotype in a particular environment. Often expressed relative to another genotype, such as the ancestor in evolution experiments.

RANDOM DRIFT

The change in frequency of genotypes in a population that is caused by chance differences in survival and reproduction, as opposed to consistent differences in their fitness.

REPLICATE POPULATIONS

Two or more populations that started from the same ancestral genotype and were propagated under identical conditions as part of an evolution experiment. By having replicates in each of several environments, it is possible to distinguish statistically between systematic responses of the populations to a particular environmental feature (for example, temperature) and other responses that might reflect the chance effects of mutation and drift.

ISOGENIC

Genotypes that have been engineered to be identical, with the exception of one or more mutations of interest.

HITCHHIKING

The process by which a neutral, or even deleterious, mutation increases in frequency owing to its physical linkage with a beneficial mutation elsewhere in the genome.

EPISTASIS

Any non-additive interaction between two or more mutations at different loci, such that their combined effect on a phenotype deviates from the sum of their individual effects.

SERIAL TRANSFER

A culture regime in which some proportion of a population is periodically diluted into fresh medium, in which the population grows until it exhausts the limiting resource and then waits until the next transfer cycle. Selection favours rapid exponential growth as well as the ability to respond quickly following transfer into fresh medium.

CHEMOSTAT

A device that allows the continuous growth of a bacterial population on a growth-rate-limiting resource. The resource flows into the chemostat at a constant rate; depleted medium and cells are washed out at the same rate. The population grows and consumes the resource until the bacteria reach an equilibrium density at which their growth rate equals the flow rate through the vessel.

PORIN

A protein channel across the outer membrane of a Gram-negative bacterium that allows the diffusion of molecules into the periplasm, which is located between the outer and inner membranes.

STATIONARY PHASE

The period in a serial-transfer regime after the limiting resource has been depleted, such that population growth ceases. A population can be kept in this phase indefinitely by never transferring it to fresh medium, and it eventually declines owing to starvation.

PLEIOTROPY

The side-effect of a mutation that affects a primary trait or function on a secondary trait or function.

BOTTLENECK

A severe reduction in population size that causes the loss of genetic variation. The role of random drift is increased, whereas the power of selection is reduced, by bottlenecks.

AUXOTROPHIC

A mutant that cannot synthesize a required nutrient, such as an amino acid.

GENETIC LOAD

The loss of fitness that is caused by producing offspring that carry deleterious mutations, and the resulting decrease in the rate of population growth.

SEQUENCE SPACE

The universe of all possible sequences or genotypes. For example, even a small viral genome of 1,000 nucleotides has 3,000 one-step neighbours, nearly 9,000,000 two-step neighbours, and more than 10600 variants at all possible distances of the same genome length.

DIGITAL ORGANISMS

A type of computer-based artificial life that can be used to investigate certain scientific questions. The genomes of digital organisms are computer programs and, like computer viruses, are able to self-replicate. Digital organisms can also mutate and evolve spontaneously, whereas computer viruses are deliberately modified by hackers.

CHAPERONES

A class of protein that binds to other proteins and thereby promotes their proper folding during synthesis or following damage.

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Elena, S., Lenski, R. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet 4, 457–469 (2003). https://doi.org/10.1038/nrg1088

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