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Evolutionary rescue from extinction is contingent on a lower rate of environmental change

Nature volume 494, pages 463–467 (2013)Cite this article

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Abstract

The extinction rate of populations is predicted to rise under increasing rates of environmental change1,2,3. If a population experiencing increasingly stressful conditions lacks appropriate phenotypic plasticity or access to more suitable habitats, then genetic change may be the only way to avoid extinction1. Evolutionary rescue from extinction occurs when natural selection enriches a population for more stress-tolerant genetic variants1,3. Some experimental studies have shown that lower rates of environmental change lead to more adapted populations or fewer extinctions4,5,6,7,8,9. However, there has been little focus on the genetic changes that underlie evolutionary rescue. Here we demonstrate that some evolutionary trajectories are contingent on a lower rate of environmental change. We allowed hundreds of populations of Escherichia coli to evolve under variable rates of increase in concentration of the antibiotic rifampicin. We then genetically engineered all combinations of mutations from isolates evolved under lower rates of environmental change. By assessing fitness of these engineered strains across a range of drug concentrations, we show that certain genotypes are evolutionarily inaccessible under rapid environmental change. Rapidly deteriorating environments not only limit mutational opportunities by lowering population size, but they can also eliminate sets of mutations as evolutionary options. As anthropogenic activities are leading to environmental change at unprecedented rapidity1, it is critical to understand how the rate of environmental change affects both demographic and genetic underpinnings of evolutionary rescue.

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Figure 1: Survival and growth under different rates of environmental change.
Figure 2: Mutations and their effects.
Figure 3: A two-locus biallelic example illustrating historical contingency upon the environment.
Figure 4: Selective accessibility from the ancestral genotype to two evolved genotypes in two different Gradual populations.

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Acknowledgements

We thank T. Bradshaw, J. Martiny and J. Tewksbury for sharing ideas that inspired this work; the Church laboratory for supplying the pKOV vector; C. Adams, S. DeCew, K. Dickinson, S. Drescher, C. Eshelman, K. Hobbs, C. Muerdter, B. Rogers and C. Shyue for help in the laboratory; and F. Bertels, C. Eshelman, C. Glenney and S. Singhal for comments on the manuscript. This material is based in part on work supported by the National Science Foundation under Cooperative Agreement Number DBI-0939454, a NSF CAREER Award Grant (DEB0952825), and a UW Royalty Research Fund Award (A74107).

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Authors and Affiliations

  1. Department of Biology and BEACON Center for the Study of Evolution in Action, University of Washington, Seattle, 98195, Washington, USA

    Haley A. Lindsey, Jenna Gallie, Susan Taylor & Benjamin Kerr

  2. Department of Environmental Microbiology, Eawag, 8600, Dübendorf, Switzerland

    Jenna Gallie

  3. Department of Environmental Systems Science, ETH Zurich, 8092, Zurich, Switzerland

    Jenna Gallie

Authors
  1. Haley A. Lindsey
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  2. Jenna Gallie
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  3. Susan Taylor
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  4. Benjamin Kerr
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Contributions

B.K. and S.T. designed the evolution experiment; S.T. and H.A.L. performed the evolution experiment; all authors designed and troubleshot the genetic and phenotypic protocols; H.A.L. performed the genetic work and phenotypic assays; B.K. did the mathematical and statistical analysis, and all authors contributed to the writing of the manuscript.

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Correspondence to Benjamin Kerr.

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The authors declare no competing financial interests.

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This file contains Supplementary Methods, Supplementary Results and Data, Supplementary Tables 1-2 and Supplementary Figures 1-3. (PDF 608 kb)

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Lindsey, H., Gallie, J., Taylor, S. et al. Evolutionary rescue from extinction is contingent on a lower rate of environmental change. Nature 494, 463–467 (2013). https://doi.org/10.1038/nature11879

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