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Diminishing-returns epistasis decreases adaptability along an evolutionary trajectory

Nature Ecology & Evolution volume 1, Article number: 0061 (2017) Cite this article

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Abstract

Populations evolving in constant environments exhibit declining adaptability. Understanding the basis of this pattern could reveal underlying processes determining the repeatability of evolutionary outcomes. In principle, declining adaptability can be due to a decrease in the effect size of beneficial mutations, a decrease in the rate at which they occur, or some combination of both. By evolving Escherichia coli populations started from different steps along a single evolutionary trajectory, we show that declining adaptability is best explained by a decrease in the size of available beneficial mutations. This pattern reflected the dominant influence of negative genetic interactions that caused new beneficial mutations to confer smaller benefits in fitter genotypes. Genome sequencing revealed that starting genotypes that were more similar to one another did not exhibit greater similarity in terms of new beneficial mutations, supporting the view that epistasis acts globally, having a greater influence on the effect than on the identity of available mutations along an adaptive trajectory. Our findings provide support for a general mechanism that leads to predictable phenotypic evolutionary trajectories.

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Figure 1: Estimation of evolutionary parameters along an adaptive trajectory.
Figure 2: Mutations in clones isolated from replay populations started from each founder.
Figure 3: Fitness effect of mutations isolated from replay populations started from the Ev 5 founder when transferred individually into the ancestor and the Ev 5 founder.
Figure 4: Effect of founder genotype on identity of mutations occurring in replay populations.

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Acknowledgements

This work was supported by a grant from the National Science Foundation (DEB-1253650 to T.F.C).

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Author notes

  1. Duy M. Dinh, Rebecca S. Satterwhite, Carolina Diaz Arenas & Daniel M. Stoebel

    Present address: ‡Present addresses: Division of Geographic Medicine and Infectious Diseases, Tufts Medical Center, Boston, Massachusetts 02111, USA (D.M.D); Department of Ecology and Evolution, University of Chicago, Chicago, Illinois 60637, USA (R.S.S); Nucleic Acid Chemistry and Engineering, Okinawa Institute of Science and Technology, Okinawa 904-0495, Japan (C.D.A); Department of Biology, Harvey Mudd College, Claremont, California 91711, USA (D.M.S).,

  2. Andrea Wünsche and Duy M. Dinh: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology and Biochemistry, University of Houston, Houston, 77204, Texas, USA

    Andrea Wünsche, Duy M. Dinh, Rebecca S. Satterwhite, Carolina Diaz Arenas, Daniel M. Stoebel & Tim F. Cooper

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Contributions

T.F.C. conceived and designed the study, and performed analyses. A.W., D.M.D., R.S.S., C.D.A. and D.M.S. performed the experiments. All authors contributed to the writing of the paper.

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Correspondence to Tim F. Cooper.

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The authors declare no competing financial interests.

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Supplementary Information

Supplementary Tables 1–5; Supplementary Figures 1–6 (PDF 2165 kb)

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Wünsche, A., Dinh, D., Satterwhite, R. et al. Diminishing-returns epistasis decreases adaptability along an evolutionary trajectory. Nat Ecol Evol 1, 0061 (2017). https://doi.org/10.1038/s41559-016-0061

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