Effects of Four Nematode Species on Fitness Costs of Pink Bollworm Resistance to Bacillus thuringiensis Toxin Cry1Ac

Abstract

Evolution of resistance by pests can reduce the efficacy of transgenic crops that produce insecticidal toxins from the bacterium Bacillus thuringiensis Berliner (Bt). In conjunction with refuges of non-Bt host plants, fitness costs can delay the evolution of resistance. Furthermore, fitness costs often vary with ecological conditions, suggesting that agricultural landscapes can be manipulated to magnify fitness costs and thereby prolong the efficacy of Bt crops. In the current study, we tested the effects of four species of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) on the magnitude and dominance of fitness costs of resistance to Bt toxin CrylAc in pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae). For more than a decade, field populations of pink bollworm in the United States have remained susceptible to Bt cotton Gossypium hirsutum L. producing CrylAc; however, we used laboratory strains that had a mixture of susceptible and resistant individuals. In laboratory experiments, dominant fitness costs were imposed by the nematodeSteinernema riobrave Cabanillas, Poinar, and Raulston but no fitness costs were imposed bySteinernema carpocapsae Weiser, Steinernema sp. (ML18 strain), or Heterorhabditis sonorensis Stock, Rivera-Orduño, and Flores-Lara. In computer simulations, evolution of resistance to CrylAc by pink bollworm was substantially delayed by treating some non-Bt cotton refuge fields with nematodes that imposed a dominant fitness cost, similar to the cost observed in laboratory experiments with S. riobrave. Based on the results here and in related studies, we conclude that entomopathogenic nematodes could bolster insect resistance management, but the success of this approach will depend on selecting the appropriate species of nematode and environment, as fitness costs were magnified by only two of five species evaluated and also depended on environmental factors. RightsWorks produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The content of this document is not copyrighted. ABSTRACT Evolution of resistance by pests can reduce the efÞcacy of transgenic crops that produce insecticidal toxins from the bacterium Bacillus thuringiensis Berliner (Bt). In conjunction with refuges of non-Bt host plants, Þtness costs can delay the evolution of resistance. Furthermore, Þtness costs often vary with ecological conditions, suggesting that agricultural landscapes can be manipulated to magnify Þtness costs and thereby prolong the efÞcacy of Bt crops. In the current study, we tested the effects of four species of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) on the magnitude and dominance of Þtness costs of resistance to Bt toxin Cry1Ac in pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae). For more than a decade, Þeld populations of pink bollworm in the United States have remained susceptible to Bt cotton Gossypium hirsutum L. producing Cry1Ac; however,...

Effects of Entomopathogenic Nematodes on Evolution of Pink Bollworm Resistance to <I>Bacillus thuringiensis</I> Toxin Cry1Ac

“…The entomopathogenic nematode Steinernema riobrave Cabanillas, Poinar, and Raulston (Rhabditida: Steinernematidae) has been found to magnify Þtness costs in most experiments (Gassmann et al 2006(Gassmann et al , 2009bHannon et al 2010). Some experimental data also indicated that Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) magniÞed Þtness costs (Gassmann et al 2009b), but in other cases no effects on Þtness costs were detected , Hannon et al 2010. Two additional species of Steinernema and H. sonorensis Stock, Rivera-Orduñ o, and Flores-Lara were evaluated in Hannon et al (2010), but none affected Þtness costs.…”

“…Some experimental data also indicated that Heterorhabditis bacteriophora Poinar (Rhabditida: Heterorhabditidae) magniÞed Þtness costs (Gassmann et al 2009b), but in other cases no effects on Þtness costs were detected , Hannon et al 2010. Two additional species of Steinernema and H. sonorensis Stock, Rivera-Orduñ o, and Flores-Lara were evaluated in Hannon et al (2010), but none affected Þtness costs. Steinernema riobrave has been found to increase Þtness costs for pink bollworm that are homozygous for Bt resistance (i.e., recessive Þtness costs) (Gassmann et al 2006(Gassmann et al .…”

“…Steinernema riobrave has been found to increase Þtness costs for pink bollworm that are homozygous for Bt resistance (i.e., recessive Þtness costs) (Gassmann et al 2006(Gassmann et al . 2009b, and in some cases, Þtness costs were found for insects that were heterozygous for Bt resistance (i.e., nonrecessive Þtness costs) (Hannon et al 2010). Computer simulation modeling indicated that recessive costs imposed by S. riobrave could substantially prolong the efÞcacy of Cry1Ac cotton against pink bollworm if applied to all refuge Þelds (Gassmann et al , 2009b.…”

“…Computer simulation modeling indicated that recessive costs imposed by S. riobrave could substantially prolong the efÞcacy of Cry1Ac cotton against pink bollworm if applied to all refuge Þelds (Gassmann et al , 2009b. Cases of nonrecessive costs were found to be especially promising for delaying resistance (Gassmann et al 2009b, Hannon et al 2010. This is because when resistance Þrst evolves in a population, the majority of resistance alleles will be present in heterozygous individuals (Gassmann et al 2009a).…”

“…This is because when resistance Þrst evolves in a population, the majority of resistance alleles will be present in heterozygous individuals (Gassmann et al 2009a). Computer simulation modeling indicated that when only a small percentage of refuge Þeld (e.g., 2.5%) were treated with S. riobrave that imposed a nonrecessive Þtness cost, the durability of Cry1Ac cotton against pink bollworm could be increased by Ϸ50% (Hannon et al 2010).…”