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Metabolic trade-offs and the maintenance of the fittest and the flattest

Nature volume 472, pages 342346 (21 April 2011) | Download Citation

Abstract

How is diversity maintained? Environmental heterogeneity is considered to be important1, yet diversity in seemingly homogeneous environments is nonetheless observed2. This, it is assumed, must either be owing to weak selection, mutational input or a fitness advantage to genotypes when rare1. Here we demonstrate the possibility of a new general mechanism of stable diversity maintenance, one that stems from metabolic and physiological trade-offs3. The model requires that such trade-offs translate into a fitness landscape in which the most fit has unfit near-mutational neighbours, and a lower fitness peak also exists that is more mutationally robust. The ‘survival of the fittest’ applies at low mutation rates, giving way to ‘survival of the flattest’4,5,6 at high mutation rates. However, as a consequence of quasispecies-level negative frequency-dependent selection and differences in mutational robustness we observe a transition zone in which both fittest and flattest coexist. Although diversity maintenance is possible for simple organisms in simple environments, the more trade-offs there are, the wider the maintenance zone becomes. The principle may be applied to lineages within a species or species within a community, potentially explaining why competitive exclusion need not be observed in homogeneous environments. This principle predicts the enigmatic richness of metabolic strategies in clonal bacteria7 and questions the safety of lethal mutagenesis8,9 as an antimicrobial treatment.

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Acknowledgements

We thank C. Burch, M. Doebeli and T. Ferenci for discussions. L.D.H. is a Royal Society Wolfson Research Merit Award Holder, R.E.B. holds an EPSRC Leadership Fellowship, and I.G. holds a NERC Advanced Research Fellowship.

Author information

Author notes

    • Robert E. Beardmore
    •  & Ivana Gudelj

    Present address: Biosciences, Geoffrey Pope Building, Streatham Campus, University of Exeter, Exeter, Devon, EX4 4SB, UK.

    • Robert E. Beardmore
    •  & Ivana Gudelj

    These authors contributed equally to this work.

Affiliations

  1. Department of Mathematics, Imperial College London, Huxley Building, 180 Queen’s Gate, London SW7 2A7, UK

    • Robert E. Beardmore
    •  & Ivana Gudelj
  2. Department of Biology, San Diego State University, San Diego, California 92182-4614, USA

    • David A. Lipson
  3. Department of Biochemistry and Biology, University of Bath, Claverton Down, Bath, BA2 7AY, UK

    • Laurence D. Hurst

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Contributions

R.E.B. and I.G. wrote the paper, conceived the paper, designed analyses and performed analysis, D.A.L. wrote the paper and performed analysis, L.D.H. wrote the paper, conceived the paper and designed analyses.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Laurence D. Hurst.

Supplementary information

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    Supplementary Information

    This file contains Supplementary Text and Data, Supplementary Figures 1-26 with legends and additional references. See Table of Contents on page 1 for full details.

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DOI

https://doi.org/10.1038/nature09905

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