Evolution of resistance in pests can reduce the effectiveness of insecticidal proteins from Bacillus thuringiensis (Bt) produced by transgenic crops. We analyzed results of 77 studies from five continents reporting field monitoring data for resistance to Bt crops, empirical evaluation of factors affecting resistance or both. Although most pest populations remained susceptible, reduced efficacy of Bt crops caused by field-evolved resistance has been reported now for some populations of 5 of 13 major pest species examined, compared with resistant populations of only one pest species in 2005. Field outcomes support theoretical predictions that factors delaying resistance include recessive inheritance of resistance, low initial frequency of resistance alleles, abundant refuges of non-Bt host plants and two-toxin Bt crops deployed separately from one-toxin Bt crops. The results imply that proactive evaluation of the inheritance and initial frequency of resistance are useful for predicting the risk of resistance and improving strategies to sustain the effectiveness of Bt crops.
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.
Maternally inherited bacterial symbionts of arthropods are common, yet symbiont invasions of host populations have rarely been observed. Here, we show that Rickettsia sp. nr. bellii swept into a population of an invasive agricultural pest, the sweet potato whitefly, Bemisia tabaci, in just 6 years. Compared with uninfected whiteflies, Rickettsia-infected whiteflies produced more offspring, had higher survival to adulthood, developed faster, and produced a higher proportion of daughters. The symbiont thus functions as both mutualist and reproductive manipulator. The observed increased performance and sex-ratio bias of infected whiteflies are sufficient to explain the spread of Rickettsia across the southwestern United States. Symbiont invasions such as this represent a sudden evolutionary shift for the host, with potentially large impacts on its ecology and invasiveness.
Transgenic crops producing Bacillus thuringiensis (Bt) toxins for insect pest control have been successful, but their efficacy is reduced when pests evolve resistance. Here we review the definition of field-evolved resistance, the relationship between resistance and field control problems, the theory underlying strategies for delaying resistance, and resistance monitoring methods. We also analyze resistance monitoring data from five continents reported in 41 studies that evaluate responses of field populations of 11 lepidopteran pests to four Bt toxins produced by Bt corn and cotton. After more than a decade since initial commercialization of Bt crops, most target pest populations remain susceptible, whereas field-evolved resistance has been documented in some populations of three noctuid moth species: Spodoptera frugiperda (J. E. Smith) to Cry1F in Bt corn in Puerto Rico, Busseola fusca (Fuller) to CrylAb in Bt corn in South Africa, and Helicoverpa zea (Boddie) to CrylAc and Cry2Ab in Bt cotton in the southeastern United States. Field outcomes are consistent with predictions from theory, suggesting that factors delaying resistance include recessive inheritance of resistance, abundant refuges of non-Bt host plants, and two-toxin Bt crops deployed separately from one-toxin Bt crops. The insights gained from systematic analyses of resistance monitoring data may help to enhance the durability of transgenic insecticidal crops. We recommend continued use of the longstanding definition of resistance cited here and encourage discussions about which regulatory actions, if any, should be triggered by specific data on the magnitude, distribution, and impact of field-evolved resistance.
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.
Transgenic crops have revolutionized insect pest control, but their effectiveness has been reduced by evolution of resistance in pests. We analyzed global monitoring data reported during the first two decades of transgenic crops, with each case representing the responses of one pest species in one country to one insecticidal protein from Bacillus thuringiensis (Bt). The cases of pest resistance to Bt crystalline (Cry) proteins produced by transgenic crops increased from 3 in 2005 to 16 in 2016. By contrast, in 17 other cases there was no decrease in pest susceptibility to Bt crops, including the recently introduced transgenic corn that produces a Bt vegetative insecticidal protein (Vip). Recessive inheritance of pest resistance has favored sustained susceptibility, but even when inheritance is not recessive, abundant refuges of non-Bt host plants have substantially delayed resistance. These insights may inform resistance management strategies to increase the durability of current and future transgenic crops.
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