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Mutational robustness can facilitate adaptation

Abstract

Robustness seems to be the opposite of evolvability. If phenotypes are robust against mutation, we might expect that a population will have difficulty adapting to an environmental change, as several studies have suggested1,2,3,4. However, other studies contend that robust organisms are more adaptable5,6,7,8. A quantitative understanding of the relationship between robustness and evolvability will help resolve these conflicting reports and will clarify outstanding problems in molecular and experimental evolution, evolutionary developmental biology and protein engineering. Here we demonstrate, using a general population genetics model, that mutational robustness can either impede or facilitate adaptation, depending on the population size, the mutation rate and the structure of the fitness landscape. In particular, neutral diversity in a robust population can accelerate adaptation as long as the number of phenotypes accessible to an individual by mutation is smaller than the total number of phenotypes in the fitness landscape. These results provide a quantitative resolution to a significant ambiguity in evolutionary theory.

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Figure 1: The genotype–phenotype model.
Figure 2: Robustness and adaptation time.
Figure 3: Robustness and diversity.

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Acknowledgements

We thank P. Turner and members of the Plotkin laboratory for advice and feedback. J.B.P. acknowledges funding from the Burroughs Wellcome Fund, the David and Lucile Packard Foundation, the James S. McDonnell Foundation, the Alfred P. Sloan Foundation, the Defense Advanced Research Projects Agency (HR0011-05-1-0057) and the US National Institute of Allergy and Infectious Diseases (2U54AI057168). G.P.W. acknowledges funding from the John Templeton Foundation and the Perinatology Research Branch of the US National Institutes of Health.

Author Contributions J.A.D., J.B.P. and G.P.W. designed the project. J.A.D. and J.B.P. wrote the paper; G.P.W. and T.L.P. edited the paper. J.A.D. performed the simulations. T.L.P. performed most of the analysis, with contributions from J.B.P. and J.A.D. J.A.D., T.L.P. and J.B.P. wrote the Supplementary Information.

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Correspondence to Joshua B. Plotkin.

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This file contains Supplementary Data, Supplementary Figures 1-12 with Legends, Supplementary Table1 and Supplementary References. (PDF 830 kb)

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Draghi, J., Parsons, T., Wagner, G. et al. Mutational robustness can facilitate adaptation. Nature 463, 353–355 (2010). https://doi.org/10.1038/nature08694

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