Gossypol in cottonseed increases the fitness cost of resistance to Bt cotton in pink bollworm

Fitness costs of resistance to Bacillus thuringiensis (Bt) toxins can delay or counter the evolution of insect resistance to transgenic Bt crops. Here we tested the hypothesis that the plant defensive compound gossypol in cottonseed increases costs associated with resistance to Bt toxin Cry1Ac in pink bollworm (Pectinophora gossypiella), a cosmopolitan pest that feeds primarily on cottonseed. Previous work showed pink bollworm resistance to Cry1Ac produced by Bt cotton is associated with mutations disrupting a gene encoding a cadherin protein that binds Cry1Ac in susceptible larvae. We used larvae from two strains of pink bollworm, each harboring an intermediate frequency of a different cadherin allele linked with resistance. We tested larvae from both strains on two types of non-Bt cotton that differed nine-fold in the gossypol concentration in their seeds: a transgenic cultivar engineered for low gossypol production and its untransformed parental cultivar. After 10 days of larval feeding on bolls, the resistance allele frequency was significantly lower in larvae from the conventional cotton than transgenic cotton. These results imply the higher gossypol concentration in the conventional cottonseed increased the fitness cost affecting survival. Using a population genetics model, we estimated this increase in survival cost was at least 32%. We also detected a recessive fitness cost reducing larval weight in both strains of pink bollworm that did not differ between the two cotton cultivars. Designing insecticidal crops and refuge plants that exploit the vulnerability of resistant insects to plant defensive compounds could improve resistance management.