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Experimental evolution of bet hedging

Abstract

Bet hedging—stochastic switching between phenotypic states1,2,3—is a canonical example of an evolutionary adaptation that facilitates persistence in the face of fluctuating environmental conditions. Although bet hedging is found in organisms ranging from bacteria to humans4,5,6,7,8,9,10, direct evidence for an adaptive origin of this behaviour is lacking11. Here we report the de novo evolution of bet hedging in experimental bacterial populations. Bacteria were subjected to an environment that continually favoured new phenotypic states. Initially, our regime drove the successive evolution of novel phenotypes by mutation and selection; however, in two (of 12) replicates this trend was broken by the evolution of bet-hedging genotypes that persisted because of rapid stochastic phenotype switching. Genome re-sequencing of one of these switching types revealed nine mutations that distinguished it from the ancestor. The final mutation was both necessary and sufficient for rapid phenotype switching; nonetheless, the evolution of bet hedging was contingent upon earlier mutations that altered the relative fitness effect of the final mutation. These findings capture the adaptive evolution of bet hedging in the simplest of organisms, and suggest that risk-spreading strategies may have been among the earliest evolutionary solutions to life in fluctuating environments.

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Figure 1: Colony morphology evolution.
Figure 2: Link between colony and cell morphology.
Figure 4: Relative fitness of evolved and engineered strains.
Figure 3: Fitness, mutational history and effects of the carB mutation in a bet-hedging lineage.

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Acknowledgements

We thank T. F. Cooper, M. R. Goddard and D. Refardt for discussion; M. Gray, A. Hurman and G. E. M. Lamers for technical assistance; M. Ackermann, P. M. Brakefield, T. Fukami, S. Rossell and B. J. Zwaan for comments on the manuscript; T. J. M. Van Dooren for statistical advice; F. Bertels for computational analysis of Solexa data; and E. Libby for theoretical insight. This work was supported by the Marsden Fund Council from government funding administered by the Royal Society of New Zealand. H.J.E.B. is supported by a Veni Fellowship from The Netherlands Organisation for Scientific Research (NWO). J.G. was supported by a Bright Futures Scholarship from the New Zealand Foundation for Research, Science and Technology. C.K. was supported by a Feodor Lynen Fellowship from the Alexander von Humboldt Foundation, Germany. G.C.F. is supported by a Postdoctoral Fellowship from the New Zealand Foundation for Research, Science and Technology.

Author Contributions H.J.E.B. and P.B.R. conceived the research and wrote the manuscript. H.J.E.B. conducted the main selection experiment, examined the relation between cell and colony morphology, investigated reversible switching, performed genome analysis and contributed to allelic replacements. J.G. determined Cap+ cell proportions, performed transposon mutagenesis and integration-site identification, confirmed and ordered the mutations, performed allelic replacements, and contributed to fitness assays. C.K. and G.C.F. performed fitness assays. All authors commented on the manuscript

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Correspondence to Hubertus J. E. Beaumont.

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This file contains Supplementary Notes 1- 4, Supplementary Methods 1-2, Supplementary Table 1 and Supplementary Figure S1 with Legend. (PDF 140 kb)

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Beaumont, H., Gallie, J., Kost, C. et al. Experimental evolution of bet hedging . Nature 462, 90–93 (2009). https://doi.org/10.1038/nature08504

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