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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.

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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.

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Correspondence to Anurag A. Agrawal or Ralph Tollrian.

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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.

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