Evolution of resistance by insect pests threatens the continued effectiveness of Bacillus thuringiensis (Bt) toxins in sprays and transgenic crops. Fitness costs of Bt resistance occur when, in the absence of Bt toxins, fitness is lower for resistant insects than for susceptible insects. Modeling results show that fitness costs can delay resistance by selecting against Bt-resistant genotypes in refuges where insects are not exposed to Bt toxins. In 77 studies including 18 species, fitness costs were detected in 62% of experiments testing for declines in resistance and in 34% of fitness component comparisons. Mean fitness costs were 15.5% for survival, 7.4% for development time, and 2.5% for mass. Although most fitness costs were recessive, nonrecessive costs can select more strongly against resistance. Because fitness costs vary with ecological conditions, refuges designed to increase the dominance or magnitude of fitness costs could be especially useful for delaying pest resistance.

Evolution of insect resistance threatens the continued success of transgenic crops producing Bacillus thuringiensis (Bt) toxins that kill pests. The approach used most widely to delay insect resistance to Bt crops is the refuge strategy, which requires refuges of host plants without Bt toxins near Bt crops to promote survival of susceptible pests. However, large-scale tests of the refuge strategy have been problematic. Analysis of more than a decade of global monitoring data reveals that the frequency of resistance alleles has increased substantially in some field populations of Helicoverpa zea, but not in five other major pests in Australia, China, Spain and the United States. The resistance of H. zea to Bt toxin Cry1Ac in transgenic cotton has not caused widespread crop failures, in part because other tactics augment control of this pest. The field outcomes documented with monitoring data are consistent with the theory underlying the refuge strategy, suggesting that refuges have helped to delay resistance.

BackgroundCrops engineered to produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) are planted on millions of hectares annually, reducing the use of conventional insecticides and suppressing pests. However, the evolution of resistance could cut short these benefits. A primary pest targeted by Bt maize in the United States is the western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae).Methodology/Principal FindingsWe report that fields identified by farmers as having severe rootworm feeding injury to Bt maize contained populations of western corn rootworm that displayed significantly higher survival on Cry3Bb1 maize in laboratory bioassays than did western corn rootworm from fields not associated with such feeding injury. In all cases, fields experiencing severe rootworm feeding contained Cry3Bb1 maize. Interviews with farmers indicated that Cry3Bb1 maize had been grown in those fields for at least three consecutive years. There was a significant positive correlation between the number of years Cry3Bb1 maize had been grown in a field and the survival of rootworm populations on Cry3Bb1 maize in bioassays. However, there was no significant correlation among populations for survival on Cry34/35Ab1 maize and Cry3Bb1 maize, suggesting a lack of cross resistance between these Bt toxins.Conclusions/SignificanceThis is the first report of field-evolved resistance to a Bt toxin by the western corn rootworm and by any species of Coleoptera. Insufficient planting of refuges and non-recessive inheritance of resistance may have contributed to resistance. These results suggest that improvements in resistance management and a more integrated approach to the use of Bt crops may be necessary.

Significance Crops genetically engineered to produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) kill pest insects and reduce the use of conventional insecticides. However, the evolution of Bt resistance can diminishes these benefits. The western corn rootworm is a serious pest of maize and is managed with Bt maize. Beginning in 2009, western corn rootworm with resistance to maize producing the Bt toxin Cry3Bb1 imposed severe injury to Cry3Bb1 maize in Iowa. We show that cross-resistance exists between Cry3Bb1 maize and mCry3A maize and is associated with severe injury to Bt maize in farmers’ fields. These results illustrate that Bt crops producing less than a high dose of toxin against target pests may select for resistance rapidly; consequently, current approaches for managing Bt resistance should be reexamined.

Background: Crops engineered to produce insecticidal toxins derived from the bacterium Bacillus thuringiensis (Bt) are planted on millions of hectares annually, reducing the use of conventional insecticides and suppressing pests. However, the evolution of resistance could cut short these benefits. A primary pest targeted by Bt maize in the United States is the western corn rootworm Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae).

Transgenic plants have been widely adopted by growers to manage the western corn rootworm, Diabrotica virgifera virgifera LeConte, in field corn. Because of reduced efficacy in some Nebraska fields after repeated use of Cry3Bb1-expressing hybrids, single plant bioassays were conducted in 2012 and 2013 to characterize the susceptibility of western corn rootworm populations to the rootwormactive proteins Cry3Bb1, mCry3A, and Cry34/35Ab1. Results demonstrate that there are heritable differences in susceptibility of Nebraska western corn rootworm populations to rootworm-active Bt traits. Proportional survival and corrected survival data coupled with field histories collectively support the conclusion that a level of field resistance to Cry3Bb1 has evolved in some Nebraska populations in response to selection pressure and that cross-resistance exists between Cry3Bb1 and mCry3A. There was no apparent cross-resistance between Cry34/35Ab1 and either Cry3Bb1 or mCry3A. The potential implications of these results on current and future corn rootworm management strategies are discussed.

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