1. In this essay I summarize current trends in the evolutionary ecology of plant defence, while advocating for approaches that integrate community ecology with specific tests of classic evolutionary hypotheses. Several conclusions emerge.
2. The microevolution of defence is perhaps best studied by reciprocal transplant experiments of differentiated plant populations while simultaneously manipulating the presence of the herbivore(s) hypothesized to be the agent(s) of natural selection.
3. Although there is continued interest in the costs of defence, I argue that some empirical approaches to estimating costs (e.g. genetic engineering) may provide limited insight into evolutionary processes.
4. Essentially all plants employ several different lines of defence against herbivory. It is thus time to abandon searching for single silver bullet traits and the simple trade-off model (where traits are arbitrarily expected to negatively covary across genotypes or species). We still know very little about which trait combinations are most effective and have repeatedly evolved together. Thus, some of our prominent theories (e.g. a predicted trade-off between direct and indirect defence) need to be revised.
5. Studies of the macroevolution of plant defence are enjoying renewed interest due to available phylogenies and analytical methods. Although general trends are not currently surmisable, we will soon have strong case studies evaluating both biotic and abiotic drivers of convergent evolution in defence strategies and the role of defence evolution in the adaptive radiation of plant lineages.
6. The evolution of specificity is proposed as a final frontier in understanding complexity in plant–herbivore interactions. Although it is abundantly clear that plants can deploy highly specific defensive responses that are differentially perceived by herbivore species, how such responses evolve and are physiologically regulated remains an important gap. Relatively straightforward methodologies are now available to close the loop between plant perception of herbivory, hormonal responses, and production of defensive end-products across genotype or species.