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.

  • Review Article
  • Published:

Co-evolution and plant resistance to natural enemies

Nature volume 411, pages 857–864 (2001)Cite this article

Abstract

Co-evolution between plants and their natural enemies is generally believed to have generated much of the Earth's biological diversity. A process analogous to co-evolution occurs in agricultural systems, in which natural enemies adapt to crop resistance introduced by breeding or genetic engineering. Because of this similarity, the investigation of resistance mechanisms in crops is helping to elucidate the workings of co-evolution in nature, while evolutionary principles, including those derived from investigation of co-evolution in nature, are being applied in the management of resistance in genetically engineered crops.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic portrayal of the HDR strategy.

Similar content being viewed by others

References

  1. Ehrlich, P. R. & Raven, P. H. Butterflies and plants: a study in coevolution. Evolution 18, 586–608 (1964).

    Google Scholar 

  2. Thompson, J. N. The Coevolutionary Process (Univ. of Chicago Press, Chicago, 1994).

    Google Scholar 

  3. Whittaker, R. H. & Feeny, P. P. Allelochemics: chemical interactions between species. Science 171, 757–770 (1971).

    ADS  CAS  PubMed  Google Scholar 

  4. Janzen, D. H. When is it coevolution? Evolution 34, 611–612 (1980).

    PubMed  Google Scholar 

  5. Gould, F. in Chemical Mediation of Coevolution (ed. Spencer, K. C.) 13–55 (Academic Press, New York, 1988).

    Google Scholar 

  6. Berenbaum, M. R. & Zangerl, A. R. in Chemical Mediation of Coevolution (ed. Spencer, K. C.) 113–132 (Academic Press, New York, 1988).

    Google Scholar 

  7. Rausher, M. D. in Evolutionary Perspectives in Insect Chemical Ecology (eds Roitberg, B. D. & Isman, M. B.) 20–88 (Routledge, Chapman & Hall, New York, 1992).

    Google Scholar 

  8. Hatchett, J. H. & Gallun, R. L. Frequency of Hessian fly, Mayteiola destructor, races in field populations. Ann. Entomol. Soc. Am. 61, 1446–1449 (1968).

    Google Scholar 

  9. Gallun, R. L. Genetic basis of Hessian fly epidemics. Ann. NY Acad. Sci. 287, 223–229 (1977).

    ADS  Google Scholar 

  10. Foster, J. E., Ohm, H. W., Patterson, F. L. & Taylor, P. L. Effectiveness of deploying single gene resistances in wheat for controlling damage by the Hessian fly (Diptera: Cecidomyiidae). Environ. Entomol. 20, 964–969 (1991).

    Google Scholar 

  11. Rosenthal, G. A., Dahlman, D. L. & Janzen, D. H. A novel means for dealing with L-canavanine, a toxic metabolite. Science 192, 256–258 (1976).

    ADS  CAS  PubMed  Google Scholar 

  12. 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  PubMed  PubMed Central  Google Scholar 

  13. Shirley, B. W. Flavonoid biosynthesis: 'new' functions for an old pathway. Trends Plant Sci. 11, 377–382 (1996).

    Google Scholar 

  14. Muller, C. H. The “co-” in coevolution. Science 164, 197–198 (1969).

    ADS  CAS  PubMed  Google Scholar 

  15. Robinson, T. Metabolism and function of alkaloids in plants. Science 184, 430–435 (1974).

    ADS  CAS  PubMed  Google Scholar 

  16. Seigler, D. & Price, P. W. Secondary compounds in plants: primary functions. Am. Nat. 110, 101–105 (1976).

    CAS  Google Scholar 

  17. Koes, R. E., Quattrocchio, F. & Mol, J. N. M. The flavonoid biosynthetic pathway in plants: function and evolution. BioEssays 16, 123–132 (1994).

    CAS  Google Scholar 

  18. Seigler, D. S. Primary roles for secondary compounds. Biochem. System. Ecol. 5, 195–199.

    CAS  Google Scholar 

  19. Jermy, T. Insect–host-plant relationship - co-evolution or sequential evolution? Symp. Biol. Hung. 16, 109–113 (1976).

    Google Scholar 

  20. Jermy, T. Evolution of insect/host plant relationships. Am. Nat. 124, 609–630 (1984).

    Google Scholar 

  21. Rausher, M. D. Genetic analysis of coevolution between plants and their natural enemies. Trends Genet. 12, 212–217 (1996).

    CAS  PubMed  Google Scholar 

  22. Strong, D. R., Lawton, J. H. & Southwood, R. Insects on Plants (Harvard Univ. Press, Cambridge, MA, 1984).

    Google Scholar 

  23. Bernays, E. & Graham, M. On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886–892 (1988).

    Google Scholar 

  24. Mauricio, R. & Rausher, M. D. Experimental manipulation of putative selective agents provides evidence for the role of natural enemies in the evolution of plant defense. Evolution 51, 1435–1444 (1997).

    PubMed  Google Scholar 

  25. Schonle, I. & Bergelson, J. Evolutionary ecology of the tropane alkaloids of Datura stramonium L. (Solanaceae). Evolution 54, 778–788 (2000).

    Google Scholar 

  26. Biere, A. & Antonovics, J. Sex-specific costs of resistance to the fungal pathogen Ustilago violacea (Microbotryum violaceum) in Silene alba . Evolution 50, 1098–1110 (1996).

    PubMed  Google Scholar 

  27. Simms, E. L. & Rausher, M. D. The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43, 573–585 (1989).

    PubMed  Google Scholar 

  28. Tiffin, P. & Rausher, M. D. Genetic constraints and selection acting on tolerance to herbivory in the common morning glory, Ipomoea purpurea . Am. Nat. 154, 700–716 (1999).

    PubMed  Google Scholar 

  29. Parker, J. E. & Coleman, M. J. Molecular intimacy between proteins specifying plant-pathogen recognition. Trends Biochem. Sci. 22, 291–296 (1997).

    CAS  PubMed  Google Scholar 

  30. Hammond-Kosack, K. E. & Jones, J. D. G. Resistance gene-dependent plant defense responses. Plant Cell 8, 1773–1791 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. De Wit, P. J. G. M. Pathogen avirulence and plant resistance: a key role for recognition. Trends Plant Sci. 2, 452–458 (1997).

    Google Scholar 

  32. Parniske, M. et al. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell 91, 821–832 (1997).

    CAS  PubMed  Google Scholar 

  33. Wang, G.-L. et al. Xa21D encodes a receptor-like molecular with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10, 765–779 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Meyers, B. C., Shen, K. A., Rohani, P., Gaut, B. S. & Michelmore, R. W. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell 11, 1833–1846 (1998).

    Google Scholar 

  35. McDowell, J. M. et al. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis . Plant Cell 10, 1861–1874 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Li, W.-H. Molecular Evolution (Sinauer, Sunderland, MA, 1997).

    Google Scholar 

  37. Bishop, J. G., Dean, A. M. & Mitchell-Olds, T. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc. Natl Acad. Sci. USA 10, 5322–5327 (2000).

    ADS  Google Scholar 

  38. Simms, E. L. in Plant Resistance to Herbivores and Pathogens: Ecology, Evolution and Genetics (eds Fritz, R. S. & Simms, E. L.) 392–425 (Univ. of Chicago Press, Chicago, 1992).

    Google Scholar 

  39. Fagerstrõm, T., Larsson, S. & Tenow, O. On optimal defense in plants. Funct. Ecol. 1, 73–81 (1987).

    Google Scholar 

  40. Simms, E. L. & Rausher, M. D. Costs and benefits of plant defense to herbivory. Am. Nat. 130, 70–581 (1987).

    Google Scholar 

  41. Berenbaum, M. R., Zangerl, A. R. & Nitao, J. K. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40, 1215–1228 (1996).

    Google Scholar 

  42. Bergelson, J. The effect of genotype and the environment on costs of resistance in lettuce. Am. Nat. 143, 349–359 (1994).

    Google Scholar 

  43. Fineblum, W. L. & Rausher, M. D. Tradeoff between resistance and tolerance to herbivore damage in a morning glory. Nature 377, 517–520 (1995).

    ADS  CAS  Google Scholar 

  44. Mauricio, R. Costs of resistance to natural enemies in field populations of the annual plant, Arabidopsis thaliana . Am. Nat. 151, 20–28 (1998).

    CAS  PubMed  Google Scholar 

  45. Bergelson, J. & Purrington, C. B. Surveying patterns in the cost of resistance in plants. Am. Nat. 148, 536–558 (1996).

    Google Scholar 

  46. Haughn, G. W. & Somerville, C. Sulfonylurea-resistant mutants of Arabidopsis thaliana . Mol. Gen. Genet. 204, 430–434 (1986).

    CAS  Google Scholar 

  47. Haughn, G. W., Smith, J., Mazur, B. & Somerville, C. Transformation with a mutant Arabidopsis acetolactate synthase gene renders tobacco resistant to sulfonylurea herbicides. Mol. Gen. Genet. 211, 266–271(1988).

    CAS  Google Scholar 

  48. Bergelson, J., Purrington, C. B., Palm, C. J. & Lopez-Guttierrez, J. C. Costs of resistance: a test using transgenic Arabidopsis thaliana . Proc. R. Soc. Lond. B 263, 1659–1663 (1996).

    ADS  CAS  Google Scholar 

  49. Purrington, C.B. & Bergelson, J. Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana . Am. Nat. 154, S82–S91 (1999).

  50. Ewald, P. W. Evolution of Infectious Disease (Oxford Univ. Press, New York, 1994).

    Google Scholar 

  51. Levin, B. R., Lipsitch, M. & Bonhoeffer, S. Population biology, evolution, and infectious disease: convergence and synthesis. Science 283, 806–809 (1999).

    CAS  PubMed  Google Scholar 

  52. Law, R. & Grey, D. R. Evolution of yields from populations with age-specific cropping. Evol. Ecol. 3, 343–359 (1989).

    Google Scholar 

  53. Heino, M. Management of evolving fish stocks. Can. J. Fish. Aquat. Sci. 55, 1971–1982 (1998).

    Google Scholar 

  54. Murphy, E. J. & Rodhouse, P. G. Rapid selection effects in a short-lived semelparous squid species exposed to exploitation: inferences from the optimisation of life-history functions. Evol. Ecol. 13, 517–537 (1999).

    Google Scholar 

  55. Hoffmann, A. A. & Parsons, P. A. Evolutionary Genetics and Environmental Stress (Oxford Univ. Press, New York, 1991).

    Google Scholar 

  56. Meefe, G. K. & Carroll, C. R. Principles of Conservation Biology 2nd edn (Sinauer, Sunderland, MA, 1997).

    Google Scholar 

  57. Landweber, L. F. & Pokrovskaya, I. D. Emergence of a dual-catalytic RNA with metal-specific cleavage and ligase activities: the spandrels of RNA evolution. Proc. Natl Acad. Sci. USA 96, 173–178 (1999).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  58. Landweber, L. F. Experimental RNA evolution. Trends Ecol. Evol. 14, 353–358 (1999).

    CAS  PubMed  Google Scholar 

  59. Proceedings of the Fourth International Meeting on DNA based Computers. Biosystems 52 (1999).

  60. Gould, F. Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu. Rev. Entomol. 43, 701–726 (1998).

    CAS  PubMed  Google Scholar 

  61. van Emden, H. F. Plant insect relationships and pest control. World Rev. Pest Control 5, 115–123 (1966).

    Google Scholar 

  62. Roush, R. T. in Advances in Insect Control: The Role of Transgenic Plants (eds Carozzi, N. & Koziel, M.) 271–294 (Taylor & Francis, London, 1997).

    Google Scholar 

  63. Environmental Protection Agency. Plant pesticides resistance management. Fed. Regist. 62(36) (1997).

  64. Fischoff, D. A. Management of lepidopteran pests with insect resistant cotton: recommended approaches. Proc. Beltwide Cotton Res. Conf. Natl Cotton Counc. Am., Memphis, TN, 751–753 (1992).

  65. Fischoff, D. A. in Biotechnology and Integrated Pest Management (ed. Persley, G. J.) 214–227 (CAB Int., Oxon, 1996).

    Google Scholar 

  66. Roush, R. T. & Plapp, F. W. Effects of insecticide resistance on biotic potential of the house fly (Musca domestica) (Diptera: Muscidae). J. Econ. Entomol. 75, 708–713 (1982).

    CAS  PubMed  Google Scholar 

  67. Fry, J. D. Trade-offs in fitness on different hosts: evidence from a selection experiment with a phytophagous mite. Am. Nat. 136, 569–580 (1990).

    Google Scholar 

  68. Groeters, F. R., Tabashnik, B. E., Finson, N. & Johnson, M. W. Fitness costs of resistance to Bacillus thuringiensis in the diamondback moth (Plutella xylostella). Evolution 48, 197–201 (1994).

    PubMed  Google Scholar 

  69. Wood, R. J. & Bishop, J. A. in Genetic Consequences of Man Made Change (eds Bishop, J. A. & Cook, L. M.) 53–96 (Academic, London, 1981).

    Google Scholar 

  70. Hamma, H., Suzuki, K. & Yanaka, H. Inheritance and stability of resistance to Bacillus thuringiensis formulations of the diamondback moth, Plutella xylostella (Linnaeus) (Lepidoptera: Yponomeutridae). Appl. Entomol. Zool. 27, 355–362 (1992).

    Google Scholar 

  71. Tabashnik, B. E., Finson, N., Groeters, F. R., Moar, W. J. & Johnson, M. W. Reversal of resistance to Bacillus thuringiensis in Plutella xylostella . Proc. Natl Acad. Sci. USA 91, 4120–4124 (1994).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  72. Perez, C. J., Shelton, A. M. & Roush, R. T. Managing diamondback moth (Lepidoptera: Plutellidae) resistance to folar applications of Bacillus thuringiensis: testing strategies in field cages. J. Econ. Entomol. 90, 1462–1470 (1997).

    Google Scholar 

  73. Liu, Y. B. & Tabashnik, B. E. Experimental evidence that refuges delay insect adaptation to Bacillus thuringiensis . Proc. R. Soc. Lond. B 264, 605–610 (1997).

    ADS  Google Scholar 

  74. Shelton, A. M., Tang, J. D., Roush, R. T., Metz, T. D. & Earle, E. D. Field tests on managing resistance to Bt-engineered plants. Nature Biotechnol. 18, 339–342 (2000).

    CAS  Google Scholar 

  75. Cox, T. S. & Hatchett, J. H.. Genetic model for wheat/Hessian fly (Diptera: Cecidomyiidae) interaction: strategies for deployment of resistance genes in wheat cultivars. Environ. Entomol. 15, 24–31 (1986).

    Google Scholar 

  76. Gould, F. The evolutionary potential of crop pests. Am. Sci. 79, 496–507 (1991).

    ADS  Google Scholar 

  77. Roush, R. T. Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil. Trans. R. Soc. Lond. B 353, 1777–1786 (1998).

    CAS  Google Scholar 

  78. Roush, R. T. Bt-transgenic crops: just another pretty insecticide or a chance for a new start in resistance management? Pesticide Sci. 51, 328–334 (1997).

    CAS  Google Scholar 

  79. Pryor, T. The origin and structure of fungal disease resistance in plants. Trends Genet. 3, 157–161 (1987).

    Google Scholar 

  80. Painter, R. Insect Resistance in Crop Plants (Wiley, New York, 1951).

    Google Scholar 

  81. Schafer, J. Tolerance to plant disease. Annu. Rev. Phytopathol. 9, 235–252 (1971).

    Google Scholar 

  82. Stowe, K. A., Marquis, R. J., Hochwender, C. G. & Simms, E. L. The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Syst. 31, 565–595 (2000).

    Google Scholar 

  83. Paige, K. N. & Whitham, D. G. Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am. Nat. 143, 739–749 (1987).

    Google Scholar 

  84. Agrawal, A. A. Overcompensation of plants in response to herbivory and the by-product benefits of mutualism Trends Plant Sci . 5, 309–313 (2000).

    CAS  PubMed  Google Scholar 

  85. Rosenthal, J. P. & Kotanen, P. M. Terrestrial plant tolerance to herbivory. Trends Ecol. Evol. 9, 145–148 (1994).

    CAS  PubMed  Google Scholar 

  86. Strauss, S. & Agrawal, A. The ecology and evolution of tolerance to herbivory. Trends Ecol. Evol. 14, 179–185 (1999).

    CAS  PubMed  Google Scholar 

  87. Tiffin, P. Are tolerance, avoidance and antibiosis evolutionarily and ecologically equivalent responses of plants to herbivores? Am. Nat. 155, 128–138 (2000).

    PubMed  Google Scholar 

  88. Futuyma, D. J. & Gould, F. Associations of plants and insects in a deciduous forest. Ecol. Monogr. 49, 33–50 (1979).

    Google Scholar 

  89. Thompson, J. N. Interaction and Coevolution. (Wiley, New York, 1982).

    Google Scholar 

  90. Bernays, E. & Graham, M. On the evolution of host specificity in phytophagous arthropods. Ecology 69, 886–892 (1988).

    Google Scholar 

  91. Rausher, M. D. in Evolution of Insect Pests: The Pattern of Variations (eds Kim, K. C & McPheron, B. A) 259–283 (Wiley, New York, 1993).

    Google Scholar 

  92. Fry, J. D. The evolution of host specialization: are trade-offs overrated? Am. Nat. 148, S84–S107 (1996).

    Google Scholar 

  93. Castillo-Chavez, C., Levin, S. A. & Gould, F. Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42, 986–994 (1988).

    PubMed  Google Scholar 

  94. Feeny, P. in Herbivores: Their Interactions with Secondary Plant Metabolites (eds Rosenthall, G. A. & Berenbaum, M.) 1–44 (Academic, San Diego, 1992).

    Google Scholar 

  95. Berenbaum, M. Coumarins and caterpillars: a case for coevolution. Evolution 37, 163–179 (1983).

    CAS  PubMed  Google Scholar 

  96. Cohen, M. B., Schuler, M. A. & Berenbaum, M. R. A host-inducible cytochrome P-450 from a host-specific caterpillar: molecular cloning and evolution. Proc. Natl Acad. Sci. USA 89, 10920–10924 (1992).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  97. Rathcke, B. J. & Poole, R. W. Coevolutionary race continues: butterfly larval adaptation to plant trichomes. Science 187, 175–176 (1975).

    ADS  CAS  PubMed  Google Scholar 

  98. Dussourd, D. E. & Eisner, T. Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237, 898–901 (1987).

    ADS  CAS  PubMed  Google Scholar 

  99. Carroll, S. P. & Loye, J. E. Specialization of Jadera species (Himiptera: Rhopalidae) on the seeds of Sapindaceae (Sapindales), and coevolutionary responses of defense and attack. Ann. Entomol. Soc. Am. 80, 373–387 (1987).

    Google Scholar 

  100. Carroll, S. P. & C. Boyd. Host race radiation in the soapberry bug: natural history with the history. Evolution 46, 1052–1069 (1992).

    PubMed  Google Scholar 

  101. Janzen, D. H. Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249–275 (1966).

    PubMed  Google Scholar 

  102. Eubanks, M. D., Nesci, K. A., Petersen, M. K., Liu, Z. & Sanchez, H. B. The exploitation of an ant-defended host plant by a shelter-building herbivore. Oecologia 109, 454–460 (1997).

    ADS  PubMed  Google Scholar 

  103. Hartl, D. L. & Clark, A. G. Principles of Population Genetics 2nd edn (Sinauer, Sunderland, MA, 1989).

    Google Scholar 

  104. Eggers-Schumacher, H. A. A comparison of the reproductive performance of insecticide-resistant and susceptible clones of Myzus persicae . Entomol. Exp. Appl. 34, 301–307 (1983).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, Evolution, Ecology and Organismal Biology Group, Duke University, Durham, 27708-0338, North Carolina, USA

    Mark D. Rausher

Authors
  1. Mark D. Rausher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark D. Rausher.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rausher, M. Co-evolution and plant resistance to natural enemies. Nature 411, 857–864 (2001). https://doi.org/10.1038/35081193

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/35081193

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

Advanced 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