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.

  • Letter
  • Published:

Transgenerational induction of defences in animals and plants

Abstract

Predators are potent agents of natural selection in biological communities. Experimental studies have shown that the introduction of predators can cause rapid evolution of defensive morphologies and behaviours in prey1,2,3,4,5 and chemical defences in plants6,7. Such defences may be constitutively expressed (phenotypically fixed) or induced when predators initially attack8,9,10. Here we show that non-lethal exposure of an animal to carnivores, and a plant to a herbivore, not only induces a defence, but causes the attacked organisms to produce offspring that are better defended than offspring from unthreatened parents. This transgenerational effect, referred to as a maternally induced defence, is in contrast to the more common defences induced in single individuals within a generation. Transgenerational induction of defences is a new level of phenotypic plasticity across generations that may be an important component of predator–prey interactions.

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

Access options

Buy this article

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

Figure 1: Raphanus raphanistrum resistance to herbivory as measured by growth of a specialist caterpillar, Pieris rapae, on the F1 generation of seedlings from different maternal environments.
Figure 2
Figure 3: Relative helmet length (mean ± s.e.) of Daphnia cucullata (F1 and F2 generation) of four treatments, organized by brood number. K, kairomone treatment (Chaoborus); C, control; K → C, mother (F0) had been transferred from kairomone to control treatment; C → K, mother (F0) had been transferred from control to kairomone treatment.

References

  1. Thompson,J. N. Rapid evolution as an ecological process. Trends Ecol. Evol. 13, 329–332 (1998).

    Article  CAS  Google Scholar 

  2. Seeley,R. H. Intense natural selection caused a rapid morphological transition in a living marine snail [Littorina obtusata]. Proc. Natl Acad. Sci. USA 83, 6897–6901 (1986).

    Article  ADS  CAS  Google Scholar 

  3. Magurran,A. E., Seghers,B. H., Carvalho,G. R. & Shaw,P. W. Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad: Evidence for the evolution of anti-predator behaviour in the wild. Proc. R. Soc. Lond. B 248, 117–122 (1992).

    Article  ADS  Google Scholar 

  4. Reznick,D. N., Shaw,F. H. Rodd,F. H. & Shaw,R. G. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275, 1934–1937 (1997).

    Article  CAS  Google Scholar 

  5. 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 

  6. Thompson,J. N. & Burdon,J. J. Gene-for-gene coevolution between plants and parasites. Nature 360, 121–125 (1992).

    Article  ADS  Google Scholar 

  7. Frita,R. S. & Simms,E. L. (eds) Plant Resistance to Herbivores and Pathogens (Univ. Chicago Press, 1992).

    Book  Google Scholar 

  8. Tollrian,R. & Harvell,C. D. (eds) The Ecology and Evolution of Inducible Defenses (Princeton Univ. Press, Princeton, NJ, 1999).

    Google Scholar 

  9. Agrawal,A. A., Tuzun,S. & Bent,E. (eds) Induced Plant Defense against Pathogens and Herbivores: Biochemistry, Ecology, and Agriculture (American Phytopathological Society Press, St Paul, Minnesota, in the press).

  10. Karban,R. & Baldwin,I. T. Induced Responses to Herbivory (Univ. Chicago Press, 1997).

    Book  Google Scholar 

  11. Agrawal,A. A. Induced responses to herbivory and increased plant performance. Science 279, 1201–1202 (1998).

    Article  ADS  CAS  Google Scholar 

  12. Mousseau,T. A. & Fox,C. W. (eds) Maternal Effects as Adaptations (Oxford Univ. Press, New York, 1998).

    Google Scholar 

  13. Rossiter,M. Incidence and consequences of inherited environmental effects. Annu. Rev. Ecol. Syst. 27, 451–476 (1996).

    Article  Google Scholar 

  14. Roach,D. A. & Wulff,R. D. Maternal effects in plants. Annu. Rev. Ecol. Syst. 18, 209–236 (1987).

    Article  Google Scholar 

  15. Schmitt,J., Niles,J. & Wulff,R. D. Norms of reaction of seed traits to maternal environments in Plantago lanceolata. Am. Nat. 139, 451–466 (1992).

    Article  Google Scholar 

  16. Tollrian,R. Predator-induced morphological defenses: Costs, life history shifts, and maternal effects in Daphnia pulex. Ecology 76, 1691–1705 (1995).

    Article  Google Scholar 

  17. Fox,C. W., Thakar,M. S. & Mousseau,T. A. Egg size plasticity in a seed beetle: An adaptive maternal effect. Am. Nat. 149, 149–163 (1997).

    Article  Google Scholar 

  18. Thiede,D. A. Maternal inheritance and its effect on adaptive evolution: A quantitative genetic analysis of maternal effects in a natural plant population. Evolution 52, 998–1015 (1998).

    Article  Google Scholar 

  19. Agrawal,A. A. Induced responses to herbivory in wild radish: Effects on several herbivores and plant fitness. Ecology 80, 1713–1723 (1999).

    Article  Google Scholar 

  20. Agrawal,A. A., Strauss,S. Y. & Stout,M. J. Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution (in the press).

  21. Hutchinson,G. E. A Treatise on Limnology Vol. 2 (Wiley, New York, 1967).

    Google Scholar 

  22. Jacobs,J. in Daphnia (eds Peters, R. H. & de Bernardi, R.) 325–252 (Memorie dell'Istituto Italiano di Idrobiologia Dott, Verbania Palanza, 1987).

  23. Tollrian,R. Predator-induced helmet formation in Daphnia cucullata (Sars). Arch. Hydrobiol. 119, 191–196 (1990).

    Google Scholar 

  24. Tolliran,R. & Von Elert,E. Enrichment and purification of Chaoborus kairomone from water: Further steps toward its chemical characterization. Limnol. Oceanogr. 39, 788–796 (1994).

    Article  ADS  Google Scholar 

  25. Schluter,D. & Gustafsson,L. Maternal inheritance of condition and clutch size in the collared flycatcher. Evolution 47, 658–667 (1993).

    Article  Google Scholar 

  26. Lenski,R. E. et al. Epistatic effects of promoter and repressor functions of the Tn10 tetracycline-resistance operon on the fitness of Escherichia coli. Mol. Ecol. 3, 127–135 (1994).

    Article  CAS  Google Scholar 

  27. Stanton,M. L. Seed variation in wild radish: Effect of seed on components of seedling and adult fitness. Ecology 65, 1105–1112 (1984).

    Article  Google Scholar 

  28. Gilbert,J. J. Rotifer ecology and embryological induction. Science 151, 1234–1237 (1966).

    Article  ADS  CAS  Google Scholar 

  29. Roberts,D. A. Acquired resistance to Tobacco Mosaic Virus transmitted to the progeny of hypersensitive tobacco. Virology 124, 161–163 (1983).

    Article  CAS  Google Scholar 

  30. Shine,R. & Downes,S. J. Can pregnant lizards adjust their offspring phenotypes to environmental conditions? Oecologia 119, 1–8 (1999).

    Article  ADS  Google Scholar 

Download references

Acknowledgements

We thank R. Karban, the plant-herbivore group at Davis and W. Gabriel for advice and encouragement; M. Morra and V. Borek for help with phytochemical analyses; R. J. Mercader, M. Kredler, S. Y. Strauss, J. Kniskern and E. Hochmuth for help with experiments; and L. S. Adler, S. Diehl, H. Dingle, R. Karban, R. E. Lenski, T. W. Schoener, S. Y. Strauss, J. S. Thaler, D. A. Thiede, and T. G. Whitham for comments on the manuscript. This work was supported by the US NSF.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Anurag A. Agrawal or Ralph Tollrian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Agrawal, A., Laforsch, C. & Tollrian, R. Transgenerational induction of defences in animals and plants. Nature 401, 60–63 (1999). https://doi.org/10.1038/43425

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/43425

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