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The role of parasites in sympatric and allopatric host diversification

An Erratum to this article was published on 16 January 2003

Abstract

Exploiters (parasites and predators) are thought to play a significant role in diversification, and ultimately speciation, of their hosts or prey1,2,3. Exploiters may drive sympatric (within-population) diversification if there are a variety of exploiter-resistance strategies or fitness costs associated with exploiter resistance4,5,6,7,8. Exploiters may also drive allopatric (between-population) diversification by creating different selection pressures and increasing the rate of random divergence9,10. We examined the effect of a virulent viral parasite (phage) on the diversification of the bacterium Pseudomonas fluorescens in spatially structured microcosms11. Here we show that in the absence of phages, bacteria rapidly diversified into spatial niche specialists with similar patterns of diversity across replicate populations. In the presence of phages, sympatric diversity was greatly reduced, as a result of phage-imposed reductions in host density decreasing competition for resources. In contrast, allopatric diversity was greatly increased as a result of phage-imposed selection for resistance, which caused populations to follow divergent evolutionary trajectories. These results show that exploiters can drive diversification between populations, but may inhibit diversification within populations by opposing diversifying selection that arises from resource competition.

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Figure 1: Partitioning of diversity.
Figure 2: Clarifying the roles of selection for resistance and density.

References

  1. Darwin, C. The Origin of Species (Thompson and Thomas, Chicago, 1872)

    Google Scholar 

  2. Lack, D. Darwin's Finches (Cambridge Univ. Press, Cambridge, 1947)

    Google Scholar 

  3. Schluter, D. Ecological character displacement in adaptive radiation. Am. Nat. 157 (suppl.), S4–S16 (2000)

    Article  Google Scholar 

  4. Holt, R. D. Predation, apparent competition, and the structure of prey communities. Theor. Pop. Biol. 12, 197–229 (1977)

    MathSciNet  CAS  Article  Google Scholar 

  5. Brown, J. S. & Vincent, T. L. Organisation of predator-prey communities as an evolutionary game. Evolution 46, 1269–1283 (1992)

    Article  Google Scholar 

  6. Schluter, D. The Ecology of Adaptive Radiations (Oxford Univ. Press, Oxford, 2000)

    Google Scholar 

  7. Abrams, P. A. Character shifts of prey species that share predators. Am. Nat. 156 (suppl.), S46–S61 (2000)

    Google Scholar 

  8. Doebeli, M. & Dieckmann, U. Evolutionary branching and sympatric speciation caused by different types of ecological interactions. Am. Nat. 156 (suppl.), S77–S101 (2000)

    Article  Google Scholar 

  9. Travis, J. The significance of geographical variation in species interactions. Am. Nat. 148 (suppl.), S1–S8 (1996)

    Article  Google Scholar 

  10. Thompson, J. N. Specific hypotheses on the geographic mosaic of coevolution. Am. Nat. 153 (suppl.), S1–S14 (1999)

    Article  Google Scholar 

  11. Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)

    ADS  CAS  Article  Google Scholar 

  12. Stone, H. M. I. On predator deterrence by pronounced shell ornament in epifaunal bivalves. Paleontology 41, 1051–1068 (1998)

    Google Scholar 

  13. Walker, J. A. Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biol. J. Linn. Soc. 61, 3–50 (1997)

    Google Scholar 

  14. Vamosi, S. M. & Schluter, D. Impacts of trout predation on the fitness of sympatric sticklebacks and their hybrids. Proc. R. Soc. Lond. B 269, 923–930 (2002)

    Article  Google Scholar 

  15. Berenbaum, M. R. & Zangerl, A. R. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl Acad. Sci. USA 95, 13743–13748 (1998)

    ADS  CAS  Article  Google Scholar 

  16. Kaltz, O. & Shykoff, J. Local adaptation in host-parasite systems. Heredity 81, 361–370 (1998)

    Article  Google Scholar 

  17. Lenski, R. E., Rose, M. R., Simpson, S. C. & Tadler, S. C. Long-term experimental evolution in Escherichia-coli. 1. Adaption and divergence during 2,000 generations. Am. Nat. 138, 1315–1341 (1991)

    Article  Google Scholar 

  18. Helling, R. B., Vargas, C. N. & Adams, J. Evolution of Escherichia coli during growth in a constant environment. Genetics 116, 349–358 (1987)

    CAS  PubMed  PubMed Central  Google Scholar 

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

    ADS  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  21. Buckling, A., Kassen, R., Bell, G. & Rainey, P. B. Disturbance and diversity in experimental microcosms. Nature 408, 961–964 (2000)

    ADS  CAS  Article  Google Scholar 

  22. Kassen, R., Buckling, A., Bell, G. & Rainey, P. B. Diversity peaks at intermediate productivity in a laboratory microcosm. Nature 406, 508–512 (2000)

    ADS  CAS  Article  Google Scholar 

  23. Ayala, F. J. & Campbell, C. A. Frequency-dependent selection. Annu. Rev. Ecol. Syst. 5, 115–138 (1974)

    Article  Google Scholar 

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

    Book  Google Scholar 

  25. Buckling, A. & Rainey, P. B. Antagonistic coevolution between a bacterium and a bacteriophage. Proc. R. Soc. Lond. B 269, 931–936 (2002)

    Article  Google Scholar 

  26. Lenski, R. E. & Levin, B. R. Constraints on the coevolution of bacteria and virulent phage—a model, some experiments, and predictions for natural communities. Am. Nat. 125, 585–602 (1985)

    Article  Google Scholar 

  27. Lande, R. Statistics and partitioning of species diversity, and similarity among multiple communities. Oikos 76, 5–13 (1996)

    Article  Google Scholar 

  28. Holt, R. D., Grover, J. & Tilman, D. Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am. Nat. 144, 741–771 (1994)

    Article  Google Scholar 

  29. Leibold, M. A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence and diversity patterns in communities. Am. Nat. 147, 784–812 (1996)

    Article  Google Scholar 

  30. Simpson, E. H. Measurement of diversity. Nature 163, 688 (1949)

    ADS  Article  Google Scholar 

Download references

Acknowledgements

We thank M. Brockhurst, L. Hurst and S. West for comments on the manuscript. This work was supported by NERC (UK) and the Royal Society.

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Correspondence to Angus Buckling.

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Buckling, A., Rainey, P. The role of parasites in sympatric and allopatric host diversification. Nature 420, 496–499 (2002). https://doi.org/10.1038/nature01164

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