Abstract
Exposure to Bacillus thuringiensis (Bt) toxins in low- and moderate-dose transgenic crops may induce sublethal effects and increase the rate of Bt resistance evolution, potentially compromising control efficacy against target pests. We tested this hypothesis using the fall armyworm Spodoptera frugiperda, a major polyphagous lepidopteran pest relatively tolerant to Bt notorious for evolving field-relevant resistance to single-gene Bt maize. Late-instar larvae were collected from Bt Cry1Ab and non-Bt maize fields in five locations in Brazil, and their offspring was compared for survival, development, and population growth in rearing environment without and with Cry1Ab throughout larval development. Larval survival on Cry1Ab maize leaves varied from 20 to 80% among the populations. Larvae reared on Cry1Ab maize had seven-day delay in development time in relation to control larvae, and such delay was shorter in offspring of armyworms from Cry1Ab maize. Population growth rates were 50–70% lower for insects continuously exposed to Cry1Ab maize relative to controls, showing the population-level effect of Cry1Ab, which varied among the populations and prior exposure to Cry1Ab maize in the field. In three out of five populations, armyworms derived from Bt maize reared on Cry1Ab maize showed higher larval weight, faster larval development and better reproductive performance than the armyworms derived from non-Bt maize, and one of these populations showed better performance on both Cry1Ab and control diets, indicating no fitness cost of the resistance trait. Altogether, these results indicate that offspring of armyworms that developed on field-grown, single-gene Bt Cry1Ab maize had reduced performance on Cry1Ab maize foliage in two populations studied, but in other three populations, these offspring had better overall performance on the Bt maize foliage than that of the armyworms from non-Bt maize fields, possibly because of Cry1Ab resistance alleles in these populations. Implications of these findings for resistance management of S. frugiperda in Bt crops are discussed.
Highlights
Sprays containing insecticidal proteins from Bacillus thuringiensis (Bt) have been used for pest management in agriculture, forestry, and public health [1]
Armyworms from Bt maize in Iguatama and Romaria produced offspring with fewer survivors than that produced from larvae collected in the non-Bt maize, indicating predominance of susceptible insects in these populations, while the opposite was observed for armyworms from Varjão de Minas, where larvae with prior exposure to Bt maize had significantly higher survival when reared on maize expressing Cry1Ab (Fig 2A)
Sublethal effects of B. thuringiensis toxins on target insects of transgenic crops have been recognized as important to interpret their population-level effects [43,44,45,46,47], studies doi:10.1371/journal.pone.0156608.g006. Integrating both lethal and sublethal effects of Bt toxins on S. frugiperda life history are scarce to date
Summary
Sprays containing insecticidal proteins from Bacillus thuringiensis (Bt) have been used for pest management in agriculture, forestry, and public health [1]. Benefits of Bt crops include effective control of target pests, decreased use of conventional insecticides, reduced impact on non-target organisms, and increased farmer profitability [5,6,7,8,9]. The long-term efficacy of Bt toxins for pest management is threatened by evolution of resistance [10, 11]. Several studies have shown the high potential for Bt resistance evolution in laboratory and natural insect populations [12,13,14,15,16], especially in pest species adapted to warm climates, where rapid selection of resistant individuals [17, 18] can lead to field-relevant resistance [19, 20], characterized by reduced pestcontrol efficacy of the Bt technology against target insects
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