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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.

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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.

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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P. Moore, S. Remold and D. Rozen for discussions; and M. Blot, D. Schneider, P. Sniegowski and V. Souza for sharing unpublished data.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.

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Correspondence to Vaughn S. Cooper.

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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

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