Historical herbivore and competitive pressure contribute to contemporary herbivore defense

Herbivory and competition are two strong selective forces on plants; however it is unclear how plants balance the competing demands of defending against multiple types of herbivores and investing in growth and reproduction. Patterns of increased competitive ability but reduced plant resistance to herbivores in natural, invaded, and managed ecosystems where herbivores are controlled or absent support evolutionary tradeoffs between growth and resistance. Here, we examine the relative contributions of selection from herbivores and competitors in shaping herbivore defense in common mustard, Brassica rapa. We used an experimental evolution approach by manipulating herbivore identity, damage, and competitive intensity to generate populations that differ in biotic history. We then tested the effect of biotic history on plant resistance to contemporary herbivores by performing bioassays with three different caterpillar species. Both historical herbivore identity and competitive history influenced contemporary resistance against herbivores in complex ways that depended on contemporary caterpillar identity. We found that for one resistance metric, time until caterpillar death, one of the three caterpillar species tested was negatively affected by past herbivory, but that the magnitude of the negative effect depended on the historical identity of the herbivore. For the other two resistance metrics we measured, time until pupation and pupal mass, we observed similar relationships between historical and contemporary herbivore identity. Surprisingly, a history of high competition lead to increased plant resistance against generalist herbivores in terms of time until pupation and pupal mass, perhaps due to a potential benefit of defense chemicals in allelopathic interactions.