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Keywords:

  • antibiosis;
  • co-evolution;
  • genetic covariance;
  • plant defence;
  • plant resistance;
  • plant-insect;
  • secondary chemistry

Summary

1. Although secondary metabolites are recognized as fundamental to the defence of plants against insect and mammalian herbivores, their relative importance compared to other potential defensive plant traits (e.g. physical resistance, gross morphology, life-history, primary chemistry and physiology) are not well understood.

2. We conducted a meta-analysis to answer the question: What types of genetically variable plant traits most strongly predict resistance against herbivores? We performed a comprehensive literature search and obtained 499 separate measurements of the strength of covariation (measured as genetic correlations) between plant traits and herbivore susceptibility – these were extracted from 72 studies involving 19 plant families.

3. Surprisingly, we found no overall association between the concentrations of secondary metabolites and herbivore susceptibility – plant traits other than secondary metabolites most strongly predicted herbivore susceptibility. Specifically, genetic variation in life-history traits (e.g. flowering time, growth rate) consistently exhibited the strongest genetic correlations with susceptibility. Genetic variation in gross morphological traits (e.g. no. branches, plant size) and physical resistance traits (e.g. latex, trichomes) were also frequently correlated with variation in herbivore susceptibility, but these relationships depended on attributes of the herbivores (e.g. feeding guild) and plants (e.g. longevity).

4. These results call into question the conventional wisdom that secondary metabolites are the most important anti-herbivore defence of plants. We propose the hypothesis that herbivores select most strongly on genetic variation in life-history, morphological and physical resistance traits, but the greater pleiotropic effects of genes controlling these traits impose strong constraints on their evolution. Meanwhile, secondary metabolites could have evolved to be important defensive mechanisms not because they have the largest effect on herbivores, but because the constraints on their evolution are the weakest.