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

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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Figure 1: Maintenance of the fittest and flattest with known parameter values.
Figure 2: The maintenance of the fittest and the flattest is not a simple mutation–selection equilibrium.
Figure 3: Quasispecies negative frequency-dependent selection.

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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.

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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.

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Correspondence to Laurence D. Hurst.

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The authors declare no competing financial interests.

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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. (PDF 1496 kb)

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Beardmore, R., Gudelj, I., Lipson, D. et al. Metabolic trade-offs and the maintenance of the fittest and the flattest. Nature 472, 342–346 (2011). https://doi.org/10.1038/nature09905

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