Submitted to: Journal of Economic Entomology
Publication Type: Peer reviewed journal
Publication Acceptance Date: 2/29/2012
Publication Date: 6/1/2012
Citation: Gassmann, A., Hannon, E.R., Sisterson, M.S., Stock, P., Carriere, Y., Tabashnik, B. 2012. Effects of entomopathogenic nematodes on the evolution of pink bollworm resistance to Bt toxin Cry1Ac. Journal of Economic Entomology. 105:994-1005. Interpretive Summary: Transgenic crops producing insecticidal toxins from the bacterium Bacillus thuringiensis (Bt) are cultivated throughout the world. Large-scale planting of Bt crops places strong selection on pests to evolve resistance. To delay the evolution of resistance growers are required to plant refuges of conventional varieties. Application of biological agents to refuges that magnify fitness costs associated with resistance could increase the effectiveness of the refuge strategy. The entomopathogenic nematode Steinernema riobrave causes greater mortality to pink bollworm (Pectinophora gossypiella) larvae carrying Bt resistance alleles than to pink bollworm larvae that are susceptible to Bt toxin. Two selection experiments were conducted to determine whether application of nematodes may help delay resistance. The first experiment was conducted in a greenhouse and found no effects of nematode application on resistance evolution. The second experiment was conducted in the laboratory and found that nematodes slowed the evolution of resistance. In both studies, the initial frequency of resistance alleles was high and populations experienced bottlenecks. A simulation model was used to evaluate the effects of using a high initial allele frequency and population bottlenecks on rates of resistance evolution in the presence and absence of fitness costs. Model results indicated that a high initial resistance allele frequency and population bottle necks diminished the ability of fitness costs to delay resistance evolution. Accordingly, the results suggest that field application of entomopathogenic nematodes may slow the evolution of resistant to Bt toxins, but only under some conditions.
Technical Abstract: The evolution of resistance by pests can reduce the efficacy of transgenic crops that produce insecticidal toxins from the bacterium Bacillus thuringiensis (Bt). Conversely, fitness costs may act to delay pest resistance to Bt. The entomopathogenic nematode Steinernema riobrave (Rhabditida: Steinernematidae) magnifies fitness costs of resistance to Bt toxin Cry1Ac in pink bollworm, Pectinophora gossypiella (Lepidoptera: Gelechiidae). Pink bollworm is a major pest of cotton in the southwestern United States that is currently managed with Bt cotton. In two selection experiments, we tested whether S. riobrave could delay the evolution of Bt resistance in pink bollworm. The first experiment was conducted in a greenhouse and the second study was conducted in a laboratory. For both experiments, hybrid lines of pink bollworm containing a mixture of alleles for resistance or susceptibility to Bt were created and exposed to a high dose / refuge scenario. In the greenhouse this was done with Bt and non-Bt cotton plants, and in the laboratory this was done with Bt and non-Bt diet. Half of the lines were exposed to S. riobrave and half were not. In the laboratory experiment, S. riobrave delayed the evolution of Bt resistance, but in the greenhouse experiment, no delay in resistance evolution was detected. We hypothesized that a high initial frequency of r-alleles and population bottlenecks lessened the ability of nematode-imposed fitness costs to delay Bt resistance in laboratory and greenhouse experiments. This hypothesis was evaluated using a simulation model parameterized based on a review of fitness costs of Bt resistance imposed on pink bollworm by S. riobrave. Modeling results demonstrate that both high r-allele frequency and population bottlenecks will diminish the ability of fitness costs to delay resistance evolution. The results suggest that field application of entomopathogenic nematodes may help mitigate the evolution of Bt resistance, but only under some conditions.