Letter | Published:

Experimental evolution of bet hedging

Nature volume 462, pages 9093 (05 November 2009) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Optimizing reproduction in a randomly varying environment. J. Theor. Biol. 12, 119–129 (1966)

  2. 2.

    & in Oxford Surveys in Evolutionary Biology, Vol. 4 (eds Harvey, P. & Partridge, L.) 182–211 (Oxford Univ. Press, 1987)

  3. 3.

    Hedging one’s evolutionary bets. Nature 250, 704–705 (1974)

  4. 4.

    et al. Self-destructive cooperation mediated by phenotypic noise. Nature 454, 987–990 (2008)

  5. 5.

    Emergence dynamics and bet hedging in a desert bee, Perdita portalis. Proc. Natl Acad. Sci. USA 266, 1985–1994 (1999)

  6. 6.

    Experimental evolution of dispersal in spatiotemporally variable microcosms. Ecol. Lett. 6, 953–959 (2003)

  7. 7.

    & The timing of copepod diapause as an evolutionary stable strategy. Am. Nat. 123, 733–751 (1984)

  8. 8.

    , , & Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4, 24–33 (1994)

  9. 9.

    Somatic generation of antibody diversity. Nature 302, 575–581 (1983)

  10. 10.

    Bet hedging in a guild of desert annuals. Ecology 88, 1086–1090 (2007)

  11. 11.

    & The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B 205, 581–598 (1979)

  12. 12.

    & Phenotypic diversity, population growth, and information in fluctuating environments. Science 309, 2075–2078 (2005)

  13. 13.

    , & Diversity in times of adversity: probabilistic strategies in microbial survival games. J. Theor. Biol. 234, 227–253 (2005)

  14. 14.

    & Fighting change with change: adaptive variation in an uncertain world. Trends Ecol. Evol. 17, 551–557 (2002)

  15. 15.

    , & Stochastic switching as a survival strategy in fluctuating environments. Nature Genet. 40, 471–475 (2008)

  16. 16.

    , , , & Bacterial persistence as a phenotypic switch. Science 305, 1622–1625 (2004)

  17. 17.

    & Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)

  18. 18.

    , , , & Adaptive divergence in experimental populations of Pseudomonas fluorescens. I. Genetic and phenotypic bases of wrinkly spreader fitness. Genetics 161, 33–46 (2002)

  19. 19.

    et al. Mutational activation of niche-specific genes provides insight into regulatory networks and bacterial function in a complex environment. Proc. Natl Acad. Sci. USA 104, 18247–18252 (2007)

  20. 20.

    , , & Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J. Bacteriol. 178, 4885–4893 (1996)

  21. 21.

    et al. Mutation discovery in bacterial genomes: metronidazole resistance in Helicobacter pylori. Nature Methods 2, 951–953 (2005)

  22. 22.

    et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53–59 (2008)

  23. 23.

    et al. Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biol. 10, R51 (2009)

  24. 24.

    et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of wrinkly spreader diversity. Genetics 176, 441–453 (2007)

  25. 25.

    et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 173, 515–526 (2006)

  26. 26.

    , , , & Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics (in the press)

  27. 27.

    , , , & Physiology and genetics of carbamoylphosphate synthesis in Escherichia coli K-12. Mol. Gen. Genet. 133, 299–316 (1974)

  28. 28.

    , & Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc. Natl Acad. Sci. USA 105, 7899–7906 (2008)

  29. 29.

    & Construction and validation of a neutrally-marked strain of Pseudomonas fluorescens SBW25. J. Microbiol. Methods 71, 78–81 (2007)

  30. 30.

    , , & Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991)

Download references

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

Author information

Author notes

    • Hubertus J. E. Beaumont
    •  & Christian Kost

    Present addresses: Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlands (H.J.E.B.); Department of Bioorganic Chemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany (C.K.).

Affiliations

  1. New Zealand Institute for Advanced Study and Allan Wilson Centre for Molecular Ecology & Evolution, Massey University, Private Bag 102904, North Shore Mail Centre, North Shore City 0745, Auckland, New Zealand

    • Hubertus J. E. Beaumont
    • , Jenna Gallie
    • , Christian Kost
    • , Gayle C. Ferguson
    •  & Paul B. Rainey
  2. Institute of Biology Leiden, Leiden University, PO Box 9505, 2300 RA Leiden, The Netherlands

    • Hubertus J. E. Beaumont

Authors

  1. Search for Hubertus J. E. Beaumont in:

  2. Search for Jenna Gallie in:

  3. Search for Christian Kost in:

  4. Search for Gayle C. Ferguson in:

  5. Search for Paul B. Rainey in:

Corresponding author

Correspondence to Hubertus J. E. Beaumont.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Notes 1- 4, Supplementary Methods 1-2, Supplementary Table 1 and Supplementary Figure S1 with Legend.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature08504

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.