Picky caterpillars: Feeding choices and adaptation to Bt crops by cotton bollworm (Helicoverpa zea)

Cotton bollworm (Helicoverpa zea) is relatively tolerant to Bt toxins and was the first insect to show field-evolved resistance to a Bt crop. To explain the relative success of this pest on Bt crops, we hypothesized that non-random feeding increases survival on Bt cotton, which heterogeneously expresses Bt toxin and nutrients in its fruiting and vegetative structures. To assess this hypothesis, cotton bollworm larvae were reared with a choice of synthetic diets containing different ratios of protein:carbohydrate (P:C) with or without the Bt toxin Cry1Ac. Both Bt-susceptible and -resistant larvae preferred an 80P:20C ratio over a 35P:65C ratio, and preferred diet lacking Bt over nutritionally identical Bt diet. However, when choosing between the 80P:20C diet with Bt toxin incorporated and the nutritionally less suitable 35P:65C diet without Bt toxin, Bt-resistant larvae showed greater preference for the toxic 80P:20C diet, while Bt-susceptible larvae preferred the non-toxic 35P:65C diet. Larvae reared in no-choice experiments had higher feeding performance on the preferred diets of each choice experiment. Our results show that cotton bollworm larvae discriminate between toxic and nutritionally unbalanced diets, making choices that maximize fitness given their genotype. In addition, Bt-resistant larvae can more successfully balance nutrient intake due to a lower need for toxin avoidance. If similar feeding choices occur on Bt plants, feeding behavior could promote adaptation to Bt crops.