Direct and indirect evolutionary effects alter ecological plant-herbivore interactions

Background/Question/Methods

Recent examples of contemporary evolution suggest that evolution might occur rapidly enough to affect the outcome of ecological interactions.   However, evolutionary effects on ecological processes are difficult to predict, in part because of indirect ecological and evolutionary effects.  We manipulated selection by invasive herbivores and competitors on populations of the native plant Lotus wrangelianus in a California grassland and allowed the populations to evolve for one generation.  Using seeds from the surviving plants, we initiated a reciprocal transplant experiment to measure how rapid evolution altered ecological interactions with insect herbivores and an exotic competitor, Medicago polymorpha, and affected Lotus fitness in different ecological contexts. 

Results/Conclusions

Ecological effects on Lotus leaf damage and fecundity were dependent on the evolutionary history of Lotus and ecological context.  In recipient environments with Medicago, the ecological effect of Medicago was strongest on: a) Lotus that had either evolved without insects or Medicago, the result of evolution mediating ecological effects, and b) Lotus that evolved with both insects and Medicago, the result of an evolutionary indirect effect.  In contrast, the evolutionary effects of both Medicago and insects typically resulted in increased damage in recipient environments where Medicago was removed, as evolutionary effects increased ecological effects, resulting in maladaptation.  Moreover, the complex interactions among competitors and herbivores appear to have prevented Lotus from adapting to Medicago; we detected evidence for local adaptation to the presence of Medicago when insect herbivore abundance was reduced with insecticide, but observed patterns of local maladaptation when insects were present.  These results suggest that explanations of ecological patterns require an understanding of evolutionary history and also illustrate the difficulty of predicting evolutionary responses in species-rich, natural communities where indirect effects are prevalent.