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“If Darwin were alive today the insect world would delight and astound him with its impressive verification of his theories of survival of the fittest. Under the stress of intensive chemical spraying the weaker members of the insect populations are being weeded out” (Carson 1962). When Rachel Carson wrote that insightful passage in Silent Spring, evolution of insecticide resistance had been documented in about 100 species of pests. In the ensuing 30 years, the number jumped to more than 500 species (Georghiou and Lagunes-Tejeda 1991). This remarkable ability of insects to adapt quickly to toxins used to control them threatens agriculture and human health worldwide (Roush and Tabashnik 1990; Denholm and Rowland 1992; Hemingway and Ranson 2000). The quantity and variety of examples of pesticide resistance also offer opportunities for determining how response to selection is affected by various factors, including behavior, dominance , fitness trade-offs, founder events, gene flow, genetic constraints, haplodiploidy, life-history traits, major and minor genes, multitrophic interactions, and population dynamics (e.g., Gould 1984; Roush and McKenzie 1987; Rosenheim and Tabashnik 1991, 1993; Carrière and Roff 1995; Carrière et al. 1995; Rosenheim et al. 1996; Bourguet and Raymond 1998; ffrench-Constant et al. 1998; Peck et al. 1999; Groeters and Tabashnik 2000; Carrière 2003; Mitchell and Onstad 2005). While study of resistance can provide fundamental insights about evolution, efforts to manage resistance enable application and testing of evolutionary theories. In particular, can strategies based on evolutionary principles delay evolution of pest resistance to insecticidal transgenic crops? Transgenic Crops with Bacillus thuringiensis (Bt) Toxins Genetic engineering creates possibilities for defending plants from herbivory with a diverse array of toxins from plants, animals, and microbes (Schuler et al. 1998; Moar 2003; Ferry et al. 2004, 2006; Cohen 2005). However, so far insecticidal crystal (Cry) proteins from the bacterium Bacillus thuringiensis (Bt) are the basis for nearly all genetically engineered crop protection against herbivorous insects in commercial agriculture. Transgenic Bt crops that kill some key pests can reduce reliance on insecticide sprays, thereby providing economic, health, and environmental benefits (Shelton et al. 2002; Carrière et al. 2003; Cattaneo et al. 2006). Evolution of resistance by pests, however, would cut short the efficacy of Bt crops and the associated benefits. First planted on a large scale in 1996, crops genetically modified to produce Bt toxins covered more than 20 million hectares worldwide during 2005, with a cumulative total of more than 120 million hectares from 1996 to 2005 (James 2005; Lawrence 2005). Although the variety of Bt toxins used in transgenic crops has increased recently (ISB 2004), cotton producing Bt toxin Cry1Ac and corn producing either Cry1Ab or Cry1Ac accounted for nearly all of the acreage of insect-protected transgenic crops grown during the past decade. These toxins kill some key lepidopteran pests of cotton and corn. Cry1Ab and Cry1Ac are so similar that evolution of resistance to one usually confers cross-resistance to the other (Tabashnik et al. 1996; Ferré and Van Rie 2002). Thus, from the standpoint of herbivore resistance, these two toxins can be considered as one type of toxin. Whereas chemically inducible Bt toxin production is feasible (Bates et al. 2005), commercially grown Bt crops produce toxin continuously. In effect, the first generation of Bt crops exposed pest populations over vast areas to a single type of Bt toxin throughout the growing season. The widespread and prolonged exposure to Bt toxins in transgenic crops represents one of the largest, most sudden selections for resistance ever seen in herbivorous insects (Tabashnik et al. 2003). Therefore, evolution of resistance by target pests is considered the primary threat to the continued 267 N I N ETE E N Evolution of Insect Resistance to Transgenic Plants BRUCE E. TABASHNIK AND YVES CARRIÈ RE success of Bt crops (Gould 1998; US EPA 2001; Ferré and Van Rie 2002; Griffitts and Aroian 2005). Resistance to a Bt toxin is a genetically based decrease in the frequency of individuals susceptible to the toxin caused by exposure of the population to the toxin (Tabashnik 1994). Many pests have quickly evolved resistance to Bt toxins in the laboratory (Tabashnik 1994; Ferré and Van Rie 2002). Furthermore, evolution of resistance to Bt sprays is documented for two lepidopteran pests of crucifers, with evidence from greenhouse populations of cabbage looper, Trichoplusia ni (Hübner) (Janmaat and Myers 2003), and field populations of diamondback moth, Plutella xylostella (L). (Tabashnik et al. 1990, 2003). Based on pervasive...


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