In pests with inherently low susceptibility to Bacillus thuringiensis (Bt) toxins, seasonal declines in the concentration of Bt toxins in transgenic crops could accelerate evolution of resistance by increasing the dominance of resistance. Here, we evaluated Helicoverpa zea survival on young and old cotton plants that produced the Bt toxins Cry1Ac and Cry1F or did not produce Bt toxins.

Extensive cultivation of crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has suppressed some major pests, reduced insecticide sprays, enhanced pest control by natural enemies, and increased grower profits. However, these benefits are being eroded by evolution of resistance in pests. We report a strategy for combating resistance by crossing transgenic Bt plants with conventional non-Bt plants and then crossing the resulting first-generation (F1) hybrid progeny and sowing the second-generation (F2) seeds. This strategy yields a random mixture within fields of three-quarters of plants that produce Bt toxin and one-quarter that does not. We hypothesized that the non-Bt plants in this mixture promote survival of susceptible insects, thereby delaying evolution of resistance. To test this hypothesis, we compared predictions from computer modeling with data monitoring pink bollworm (Pectinophora gossypiella) resistance to Bt toxin Cry1Ac produced by transgenic cotton in an 11-y study at 17 field sites in six provinces of China. The frequency of resistant individuals in the field increased before this strategy was widely deployed and then declined after its widespread adoption boosted the percentage of non-Bt cotton plants in the region. The correspondence between the predicted and observed outcomes implies that this strategy countered evolution of resistance. Despite the increased percentage of non-Bt cotton, suppression of pink bollworm was sustained. Unlike other resistance management tactics that require regulatory intervention, growers adopted this strategy voluntarily, apparently because of advantages that may include better performance as well as lower costs for seeds and insecticides.

The refuge strategy is used worldwide to delay the evolution of pest resistance to insecticides that are either sprayed or produced by transgenic Bacillus thuringiensis (Bt) crops. This strategy is based on the idea that refuges of host plants where pests are not exposed to an insecticide promote survival of susceptible pests. Despite widespread adoption of this approach, large-scale tests of the refuge strategy have been problematic. Here we tested the refuge strategy with 8 y of data on refuges and resistance to the insecticide pyriproxyfen in 84 populations of the sweetpotato whitefly (Bemisia tabaci) from cotton fields in central Arizona. We found that spatial variation in resistance to pyriproxyfen within each year was not affected by refuges of melons or alfalfa near cotton fields. However, resistance was negatively associated with the area of cotton refuges and positively associated with the area of cotton treated with pyriproxyfen. A statistical model based on the first 4 y of data, incorporating the spatial distribution of cotton treated and not treated with pyriproxyfen, adequately predicted the spatial variation in resistance observed in the last 4 y of the study, confirming that cotton refuges delayed resistance and treated cotton fields accelerated resistance. By providing a systematic assessment of the effectiveness of refuges and the scale of their effects, the spatially explicit approach applied here could be useful for testing and improving the refuge strategy in other crop-pest systems.

Development of pyriproxyfen and neonicotinoid resistance in the B-biotype whitefly and recent introduction of the Q biotype have the potential to threaten current whitefly management programs in Arizona. The possibility of integrating the novel anthranilic diamides chlorantraniliprole and cyantraniliprole into the current program to tackle these threats largely depends on whether these compounds have cross-resistance with pyriproxyfen and neonicotinoids in whiteflies. To address this question, the authors bioassayed a susceptible B-biotype strain, a pyriproxyfen-resistant B-biotype strain, four multiply resistant Q-biotype strains and 16 B-biotype field populations from Arizona with a systemic uptake bioassay developed in the present study.

Genetically engineered crops that produce insecticidal toxins from Bacillus thuringiensis (Bt) are grown widely for pest control. However, insect adaptation can reduce the toxins' efficacy. The predominant strategy for delaying pest resistance to Bt crops requires refuges of non-Bt host plants to provide susceptible insects to mate with resistant insects. Variable farmer compliance is one of the limitations of this approach. Here we report the benefits of an alternative strategy where sterile insects are released to mate with resistant insects and refuges are scarce or absent. Computer simulations show that this approach works in principle against pests with recessive or dominant inheritance of resistance. During a large-scale, four-year field deployment of this strategy in Arizona, resistance of pink bollworm (Pectinophora gossypiella) to Bt cotton did not increase. A multitactic eradication program that included the release of sterile moths reduced pink bollworm abundance by >99%, while eliminating insecticide sprays against this key invasive pest.