Resistance to dual-gene Bt maize in Spodoptera frugiperda: selection, inheritance, and cross-resistance to other transgenic events OPEN (original) (raw)

Transgenic crop " pyramids " producing two or more Bacillus thuringiensis (Bt) toxins active against the same pest are used to delay evolution of resistance in insect pest populations. Laboratory and greenhouse experiments were performed with fall armyworm, Spodoptera frugiperda, to characterize resistance to Bt maize producing Cry1A.105 and Cry2Ab and test some assumptions of the " pyramid " resistance management strategy. Selection of a field-derived strain of S. frugiperda already resistant to Cry1F maize with Cry1A.105 + Cry2Ab maize for ten generations produced resistance that allowed the larvae to colonize and complete the life cycle on these Bt maize plants. Greenhouse experiments revealed that the resistance was completely recessive (Dx = 0), incomplete, autosomal, and without maternal effects or cross-resistance to the Vip3Aa20 toxin produced in other Bt maize events. This profile of resistance supports some of the assumptions of the pyramid strategy for resistance management. However, laboratory experiments with purified Bt toxin and plant leaf tissue showed that resistance to Cry1A.105 + Cry2Ab2 maize further increased resistance to Cry1Fa, which indicates that populations of fall armyworm have high potential for developing resistance to some currently available pyramided maize used against this pest, especially where resistance to Cry1Fa was reported in the field. Transgenic crops producing toxins from the soil bacterium Bacillus thuringiensis (Bt) are a major tool for controlling insect pests worldwide 1. Benefits of Bt crops include effective management of target pests, decreased use of conventional insecticides, and reduced risks to non-target organisms, including humans 2–6. However, rapid evolution of resistance to Bt crops in several pest species has compromised some of these benefits 7,8. To increase pest control efficacy and delay resistance evolution, a gene pyramiding strategy has been employed in transgenic plants to produce two or more Bt toxins of dissimilar mode of action effective against the same target pest species 7. As a result, pyramided Bt crops have been adopted rapidly and are expected to become even more prevalent in the future 9. As a strategy for resistance management, pyramided Bt crops are expected to be more effective when insect resistance to each Bt toxin is recessive and associated with reduced fitness of resistant individuals on both non-Bt and Bt plants (i.e., with fitness costs and incomplete resistance), when selection with any one of the pyramided toxins does not cause cross-resistance to the others, and when alleles conferring resistance to each toxin are rare 10–13. However, little is known about that evolutionary response from target species to the selective pressure imposed by two or more toxins with independent mechanisms of action. In this study we characterize the inheritance of resistance to pyramided maize producing the Cry1A.105 and Cry2Ab toxins in the fall armyworm, Spodoptera frugiperda, a major migratory pest of maize in Neotropical America 14 , and recently also in southern United States 15. Previous studies with resistant strains of S. frugiperda to the event TC1507 (i.e., non-pyramided Bt maize producing the Cry1Fa toxin) showed that the genetic basis of resistance did not fit some assumptions of the high dose-refuge strategy, i.e., lack of fitness costs associated with resistance, high frequency of resistance alleles, and heterozygote survival greater than 5% on leaf tissues of Cry1F maize plants 16,17. The result has been the rather quick appearance of Cry1F resistance in Brazilian populations of the fall armyworm 16,18 .