Fitness Costs of Resistance to Bacillus thuringiensis in the Pink Bollworm Pectinophora gossypiella

Abstract

Resistance to Bacillus thuringiensis (Bt) cotton, Gossypium hirsutum, is associated with fitness costs in pink bollworm, Pectinophora gossypiella. Previous work has demonstrated that costs of resistance are induced by environmental factors including insecticidal cotton phytochemicals such as gossypol. This study (1) tested the hypothesis that the presence of toxic phytochemicals would increase the dominance and magnitude of fitness costs associated with genes conferring resistance to the Bacillus thuringiensis (Bt) toxin, (2) coupled a selection experiment and simulation modeling to evaluate the fitness cost of resistance to Bt in pink bollworm and (3) used laboratory strains containing susceptible and resistant genotypes to test the hypothesis that gossypol accumulates more readily in pink bollworm with Bt resistance alleles, and that this gossypol accumulation reduces fitness. To test hypothesis (1), larval survival and weight were measured in two independent strains of pink bollworm, Pectinophora gossypiella, reared on diet containing the cotton phytochemicals gossypol and cyclopropenoid fatty acid, alone, or in combination. Cotton phytochemicals increased the dominance and magnitude of fitness costs associated with cadherin-based resistance to Bacillus thuringiensis (Bt) toxin. Gossypol and cyclopropenoid fatty acid combined had a more detrimental effect on fitness of pink bollworm than either compound alone. To test hypothesis (2), two pink bollworm strains fed synthetic diet were monitored over 30 generations to test the hypothesis that costs associated with Bt resistance would result in a decline in the frequency of resistance. A decrease in resistance allele frequency did occur in both strains and costs affecting each resistant genotypes were estimated. To test hypothesis (3), two strains of pink bollworm were fed on diet containing gossypol and on diet without gossypol, and gossypol accumulation in tissues of genotypes was measured. In both strains, significantly more gossypol accumulated in genotypes containing at least one resistance allele and gossypol accumulation was additive to dominant. In both strains, an increase in the dominance or magnitude of costs affecting larval weight was observed on gossypol diet, and the change in the magnitude of costs was positively associated with gossypol absorption. In one strain, the presence of gossypol increased survival costs but only in the genotype with the highest gossypol absorption. The mutation conferring resistance to the Bt toxin Cry1Ac is found in the cadherin-encoding region in three lepidopeteran pests (Helicoverpa armigera, Heliothis virescens and Pectinophora gossypiella) including the pink bollworm. Cadherin proteins had been hypothesized to play a role in maintaining the integrity of the insect midgut epithelial tissue. Taken together, these results support the hypothesis that cadherin proteins do contribute to gut integrity, toxic plant phytochemicals accumulate more readily in pink bollworm with resistance alleles, and that such accumulation increases the dominance and magnitude of fitness costs.