Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The population genetics of ecological specialization in evolving Escherichia coli populations

Abstract

When organisms adapt genetically to one environment, they may lose fitness in other environments1,2,3,4. Two distinct population genetic processes can produce ecological specialization—mutation accumulation and antagonistic pleiotropy5,6,7,8. In mutation accumulation, mutations become fixed by genetic drift in genes that are not maintained by selection; adaptation to one environment and loss of adaptation to another are caused by different mutations. Antagonistic pleiotropy arises from trade-offs, such that the same mutations that are beneficial in one environment are detrimental in another. In general, it is difficult to distinguish between these processes5,6,7,8. We analysed the decay of unused catabolic functions in 12 lines of Escherichia coli propagated on glucose for 20,000 generations9,10. During that time, several lines evolved high mutation rates11. If mutation accumulation is important, their unused functions should decay more than the other lines, but no significant difference was observed. Moreover, most catabolic losses occurred early in the experiment when beneficial mutations were being rapidly fixed, a pattern predicted by antagonistic pleiotropy. Thus, antagonistic pleiotropy appears more important than mutation accumulation for the decay of unused catabolic functions in these populations.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Trajectory for mean fitness of E. coli during 20,000 generations in minimal glucose medium.
Figure 2: Hypothetical trajectories for the evolution of ecological specialization, as reflected by the decay of total catabolic function.
Figure 3: Summary of parallel changes in catabolic functions, based on comparisons between the evolved populations and common ancestor at three time points.
Figure 4: Evolution of total catabolic function during 20,000 generations in minimal glucose medium.

References

  1. 1

    Mills, D. R., Peterson, R. L. & Spiegelman, S. An extracellular Darwinian experiment with a self-duplicating nucleic acid molecule. Proc. Natl Acad. Sci. USA 58 , 217–224 (1967).

    ADS  CAS  Article  Google Scholar 

  2. 2

    Futuyma, D. J. & Moreno, G. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19, 207– 233 (1988).

    Article  Google Scholar 

  3. 3

    Fry, J. D. Tradeoffs in fitness on different hosts: evidence from a selection experiment with a phytophagous mite. Am. Nat. 136, 569–580 (1990).

    Article  Google Scholar 

  4. 4

    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  Google Scholar 

  5. 5

    Rose, M. R. & Charlesworth, B. A test of evolutionary theories of senescence. Nature 287, 141– 142 (1980).

    ADS  CAS  Article  Google Scholar 

  6. 6

    Rose, M. R. Evolutionary Biology of Aging (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  7. 7

    Holt, R. D. Demographic constraints in evolution: towards unifying the evolutionary theories of senescence and niche conservatism. Evol. Ecol. 10 , 1–11 (1996).

    Article  Google Scholar 

  8. 8

    Sgrò, C. M. & Partridge, L. A delayed wave of death from reproduction in Drosophila. Science 286, 2521–2524 (1999).

    Article  Google Scholar 

  9. 9

    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 

  10. 10

    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).

    ADS  CAS  Article  Google Scholar 

  11. 11

    Sniegowski, P. D., Gerrish, P. J. & Lenski, R. E. Evolution of high mutation rates in experimental populations of Escherichia coli. Nature 387, 703–705 (1997).

    ADS  CAS  Article  Google Scholar 

  12. 12

    Cooper, V. S. Consequences of ecological specialization in experimental long-term evolving populations of Escherichia coli. Thesis, Michigan State Univ. (2000).

  13. 13

    Kimura, M. The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, Cambridge, 1983).

    Book  Google Scholar 

  14. 14

    Miller, R. G. Simultaneous Statistical Inference (McGraw Hill, New York, 1981).

    Book  Google Scholar 

  15. 15

    Cooper, V. S., Schneider, D., Blot, M. & Lenski, R. E. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of E. coli B. J. Bacteriol. (submitted).

  16. 16

    Funchain, P. et al. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. 17

    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).

    ADS  CAS  Article  Google Scholar 

  18. 18

    Szathmáry, E. Do deleterious mutations act synergistically? Metabolic control theory provides a partial answer. Genetics 133, 127– 132 (1993).

    PubMed  PubMed Central  Google Scholar 

  19. 19

    Muller, H. J. The relation of recombination to mutational advantage. Mutat. Res. 1, 2–9 (1964 ).

    Article  Google Scholar 

  20. 20

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

    ADS  CAS  Article  Google Scholar 

  21. 21

    Houle, D., Hoffmaster, D. K., Assimacopoulos, S. & Charlesworth, B. The genomic mutation rate for fitness in Drosophila. Nature 359, 58–60 ( 1992).

    ADS  CAS  Article  Google Scholar 

  22. 22

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

    ADS  CAS  Article  Google Scholar 

  23. 23

    Biolog ES Microplate Instructions for Use (Biolog, Hayward, California, 1993).

  24. 24

    Guckert, J. B. et al. Community analysis by Biolog: curve integration for statistical analysis of activated sludge microbial habitats. J. Microb. Meth. 27, 183–197 ( 1996).

    Article  Google Scholar 

Download references

Acknowledgements

We thank L. Ekunwe for assistance; J. Conner, J. Cooper, N. Cooper, D. Futuyma, D. Hall, A. Jarosz, T. Marsh, P. Moore, S. Remold and D. Rozen for discussions; and M. Blot, D. Schneider, P. Sniegowski and V. Souza for sharing unpublished data. This research was supported by NSF grants to V.S.C. and R.E.L. and by the Center for Microbial Ecology.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Vaughn S. Cooper.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Cooper, V., Lenski, R. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407, 736–739 (2000). https://doi.org/10.1038/35037572

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing