Strong selective pressure by parasitoids mitigates the costs of consuming chemically defended plants

Co-evolutionary interactions between plants and herbivores have led to a range of plant defenses that minimize insect damage and a suite of counter-adaptations that allow herbivores to feed on defended plants. Consumption of plant secondary compounds results in herbivore growth and developmental costs but can be beneficial if eating these secondary compounds results in deterrence or harm to natural enemies.To test the role of secondary compounds on herbivore fitness in the context of natural enemies, I combined field measurements of the prevalence of a parasitoid wasp (Cotesia congregata) with detailed measurements of the costs of plant secondary compounds on growth, immune, and fitness traits across developmental stages in the herbivore Manduca sexta. When M. sexta larvae consume defended plants, Cotesia congregata are known to have reduced success. However, this anti-enemy benefit to the M. sexta host must be considered in relationship to parasitoid abundance and the type and strength of the fitness costs M. sexta incurs feeding on plant secondary compounds.I found that Cotesia congregata parasitoids exert large negative selective pressures, killing 31-57% of M. sexta larvae in the field. Manduca sexta developed fastest during the instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds (nicotine and rutin). These negative size effects at the larval stage carried over to influence adult traits associated with flight and mating but there were no immune, survival, or fecundity costs of consuming plant defensive compounds as larvae.Synthesis. These results suggest that the developmental costs experienced by M. sexta herbivores consuming defensive compounds may be outweighed by a survival benefit in the face of abundant enemy pressures.