Evolution of resistance by pests is the main threat to long-term insect control by transgenic crops that produce Bacillus thuringiensis (Bt) toxins. Because inheritance of resistance to the Bt toxins in transgenic crops is typically recessive, DNA-based screening for resistance alleles in heterozygotes is potentially much more efficient than detection of resistant homozygotes with bioassays. Such screening, however, requires knowledge of the resistance alleles in field populations of pests that are associated with survival on Bt crops. Here we report that field populations of pink bollworm (Pectinophora gossypiella), a major cotton pest, harbored three mutant alleles of a cadherinencoding gene linked with resistance to Bt toxin Cry1Ac and survival on transgenic Bt cotton. Each of the three resistance alleles has a deletion expected to eliminate at least eight amino acids upstream of the putative toxin-binding region of the cadherin protein. Larvae with two resistance alleles in any combination were resistant, whereas those with one or none were susceptible to Cry1Ac. Together with previous evidence, the results reported here identify the cadherin gene as a leading target for DNA-based screening of resistance to Bt crops in lepidopteran pests.
To delay evolution of pest resistance to transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt), the "pyramid" strategy uses plants that produce two or more toxins that kill the same pest. In the United States, this strategy has been adopted widely, with two-toxin Bt cotton replacing one-toxin Bt cotton. Although two-toxin plants are likely to be more durable than one-toxin plants, the extent of this advantage depends on several conditions. One key assumption favoring success of two-toxin plants is that they kill insects selected for resistance to one toxin, which is called "redundant killing." Here we tested this assumption for a major pest, Helicoverpa zea, on transgenic cotton producing Bt toxins Cry1Ac and Cry2Ab. Selection with Cry1Ac increased survival on two-toxin cotton, which contradicts the assumption. The concentration of Cry1Ac and Cry2Ab declined during the growing season, which would tend to exacerbate this problem. Furthermore, analysis of results from 21 selection experiments with eight species of lepidopteran pests indicates that some cross-resistance typically occurs between Cry1A and Cry2A toxins. Incorporation of empirical data into simulation models shows that the observed deviations from ideal conditions could greatly reduce the benefits of the pyramid strategy for pests like H. zea, which have inherently low susceptibility to Bt toxins and have been exposed extensively to one of the toxins in the pyramid before two-toxin plants are adopted. For such pests, the pyramid strategy could be improved by incorporating empirical data on deviations from ideal assumptions about redundant killing and cross-resistance. (Résumé d'auteur
Despite the potentially profound impact of genetically modified crops on agriculture and the environment, we know little about their long-term effects. Transgenic crops that produce toxins from Bacillus thuringiensis (Bt) to control insects are grown widely, but rapid evolution of resistance by pests could nullify their benefits. Here, we present theoretical analyses showing that long-term suppression of pest populations is governed by interactions among reproductive rate, dispersal propensity, and regional abundance of a Bt crop. Supporting this theory, a 10-year study in 15 regions across Arizona shows that Bt cotton suppressed a major pest, pink bollworm (Pectinophora gossypiella), independent of demographic effects of weather and variation among regions. Pink bollworm population density declined only in regions where Bt cotton was abundant. Such long-term suppression has not been observed with insecticide sprays, showing that transgenic crops open new avenues for pest control. The debate about putative benefits of Bt crops has focused primarily on short-term decreases in insecticide use. The present findings suggest that long-term regional pest suppression after deployment of Bt crops may also contribute to reducing the need for insecticide sprays.G enetically engineered crops have quickly become a significant component of agriculture, but little is known about their long-term consequences. Transgenic cultivars of cotton and maize that produce toxins from Bacillus thuringiensis (Bt) to control insect pests were grown on 12 million hectares worldwide during 2001 (1). A major concern is that rapid evolution of resistance by pests could nullify the benefits of Bt crops (2-6). It has also been proposed, however, that Bt crops imposing high mortality could cause regional suppression of target pests before resistance occurs (6-9). This would be most likely for target pests with a narrow host range, because their diet would be affected most by Bt crops. Here we report results of a large-scale 10-year study revealing that extensive use of Bt cotton in Arizona caused regional suppression of pink bollworm (Pectinophora gossypiella), an ecological specialist on cotton (10).Pink bollworm moths emerge in the spring, and four to five generations are completed before winter diapause begins (10). Population growth is exponential in non-Bt cotton fields where the pink bollworm is virtually always present. Survival of pink bollworm larvae is Ͻ0.5% in Bt cotton fields (3). We hypothesized that regional declines in pink bollworm density would occur because deployment of Bt cotton reduces the number of source habitats (non-Bt cotton fields) and the net reproductive rate of migrants from source habitats. Accordingly, we expected a density decline in regions where a threshold use of Bt cotton was exceeded (Fig. 1). To test this hypothesis, we evaluated changes in pink bollworm population density related to abundance of Bt cotton in each of 15 cotton-growing regions in Arizona during the 5 years before and the 5 years after deploym...
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