Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Adaptive radiation in a heterogeneous environment

Abstract

Successive adaptive radiations have played a pivotal role in the evolution of biological diversity1,2,3. The effects of adaptive radiation are often seen4,5,6, but the underlying causes are difficult to disentangle and remain unclear7,8,9. Here we examine directly therole of ecological opportunity and competition in driving genetic diversification. We use the common aerobic bacterium Pseudomonas fluorescens10, which evolves rapidly under novel environmental conditions to generate a large repertoire of mutants11,12,13. When provided with ecological opportunity (afforded by spatial structure), identical populations diversify morphologically, but when ecological opportunity is restricted there is no such divergence. In spatially structured environments, the evolution of variant morphs follows a predictable sequence and we show that competition among the newly evolved niche-specialists maintains this variation. These results demonstrate that the elementary processes of mutation and selection alone are suifficient to promote rapid proliferation of new designs and support the theory that trade-offs in competitive ability drive adaptive radiation14,15.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Phenotypic diversity and niche specificity among P. fluorescens SBW25 colonies evolved in a spatially heterogeneous environment.
Figure 2: Effect of ecological opportunity on the evolution of genetic diversity.
Figure 3: Effect of spatial heterogeneity on the maintenance of genetic variation.
Figure 4: Competitive relationships among niche-adapted classes.

References

  1. Gould, S. J. Wonderful Life: The Burgess Shale and the Nature of History (Penguin, London, 1989).

    Google Scholar 

  2. Hedges, S. B., Parker, P. H., Sibley, C. G. & Kumar, S. Continental breakup and the ordinal diversification of birds and mammals. Nature 381, 226–229 (1996).

    Article  ADS  CAS  Google Scholar 

  3. Benton, M. J. Diversification and extinction in the history of life. Science 268, 52–58 (1996).

    Article  ADS  Google Scholar 

  4. Otte, D. & Endler, J. A. (eds) Speciation and its Consequences (Sinauer, Sunderland, 1989).

    Google Scholar 

  5. Dobzhansky, T. Species of Drosophila. Science 177, 664–669 (1972).

    Article  ADS  CAS  Google Scholar 

  6. Klein, D. et al. Extensive MHC variability in cichlid fishes of Lake Malawi. Nature 364, 330–334 (1993).

    Article  ADS  CAS  Google Scholar 

  7. Schluter, D. Experimental evidence that competition promotes divergence in adaptive radiation. Science 266, 798–801 (1994).

    Article  ADS  CAS  Google Scholar 

  8. Grant, P. R. Ecology and Evolution of Darwin's Finches (Princeton Univ. Press, NJ, 1986).

    Google Scholar 

  9. Lenski, R. E. & Travisano, M. Dynamics of adaptation and diversification: a 10,000 generation experiment with bacterial populations. Proc. Natl Acad. Sci. USA 91, 6808–6814 (1994).

    Article  ADS  CAS  Google Scholar 

  10. Rainey, P. B. & Bailey, M. J. Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Mol. Microbiol. 19, 521–533 (1996).

    Article  CAS  Google Scholar 

  11. Shaprio, J. A. in The Bacteria; The Biology of Pseudomonas (ed. Sokatch, J. R.) 27–69 (Academic, London, 1986).

    Book  Google Scholar 

  12. Rainey, P. B., Moxon, E. R. & Thompson, I. P. Intraclonal polymorphism in bacteria. Adv. Microb. Ecol. 13, 263–300 (1993).

    Article  Google Scholar 

  13. Moxon, E. R., Rainey, P. B., Nowak, M. & Lenski, R. E. Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol. 4, 24–33 (1994).

    Article  CAS  Google Scholar 

  14. Taper, M. T. & Case, T. J. in Oxford Surveys in Evolutionary Biology, Vol. 8 (eds Futuyma, D. J. & Antonovics, J.) 63–109 (Oxford Univ. Press, Oxford, 1994).

    Google Scholar 

  15. Connell, J. H. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42, 710–723 (1961).

    Article  Google Scholar 

  16. Charlesworth, B., Lande, R. & Slatkin, M. Aneo-Darwinian commentary on macroevolution. Evolution 46, 16–30 (1982).

    Google Scholar 

  17. Travisano, M., Mongold, J. A., Bennett, A. F. & Lenski, R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995).

    Article  ADS  CAS  Google Scholar 

  18. Elena, M. S. F., Cooper, V. S. & Lenski, R. E. Punctuated evolution caused by selection of rare beneficial mutations. Science 272, 1802–1804 (1996).

    Article  ADS  CAS  Google Scholar 

  19. Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, Cambridge, 1995).

    Book  Google Scholar 

  20. Conway Morris, S. & Whittington, H. B. The animals of the Burgess shale. Sci. Am. 240, 122–133 (1979).

    Article  Google Scholar 

  21. Hopf, F. A., Valone, T. J. & Brown, J. H. Competition theory and the structure of ecological communities. Evol. Ecol. 7, 142–154 (1993).

    Article  Google Scholar 

  22. Bell, G. & Reboud, X. Experimental evolution in Chlamydomonas. II. Genetic variation in strongly contrasted environments. Heredity 78, 498–506 (1997).

    Article  Google Scholar 

  23. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991).

    Article  Google Scholar 

  24. Atwood, K. C., Schneider, L. K. & Ryan, F. J. Periodic selection in Escherichia coli. Proc. Natl Acad. Sci. USA 37, 146–155 (1951).

    Article  ADS  CAS  Google Scholar 

  25. Abrams, P. A. Alternative models of character displacement and niche shift. 2. Displacement when there is competition for a single resource. Am. Nat. 130, 271–282 (1987).

    Article  Google Scholar 

  26. Haldane, J. B. S. The Causes of Evolution (Longmans & Green, London, 1932).

    Google Scholar 

  27. Hedrick, P. W. Genetic polymorphism in heterogeneous environments: a decade later. Annu. Rev. Ecol. Syst. 17, 535–566 (1986).

    Article  Google Scholar 

  28. Rosenzweig, R. F., Sharp, R. R., Treves, D. S. & Adams, J. Microbial evolution in a simple unstructured environment — genetic differentiation in Escherichia coli. Genetics 137, 903–917 (1994).

    Article  CAS  Google Scholar 

  29. Turner, P. E., Souza, V. & Lenski, R. E. Tests of ecological mechanisms promoting the stable coexistence of two bacterial genotypes. Ecology 77, 2119–2129 (1996).

    Article  Google Scholar 

  30. Korona, R., Nakatsu, C. H., Forney, L. J. & Lenski, R. E. Evidence for mutliple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc. Natl Acad. Sci. USA 91, 9037–9041 (1994).

    Article  ADS  CAS  Google Scholar 

Download references

Acknowledgements

We thank K. McCallum for technical assistance; J. Baker for photography; D. Ebert, S. Kahn, B. Haubold, and E. R. Moxon for discussion; and R. E. Lenski, P. Sniegowski and I. Moore for comments ont he manuscript. This work was supported in part by grants from the B.B.S.R.C. and BTP Plc.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul B. Rainey.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rainey, P., Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998). https://doi.org/10.1038/27900

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/27900

This article is cited by

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.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing