Resistance to Bacillus thuringiensis toxins in the European corn borer: what chance for Bt maize?

Abstract

Bacillus thuringiensis (Bt) is an endospore-forming bacterium that produces a protein crystal within the cytoplasm of sporulating cells (Schnepf et al., 1998). The proteins within this crystal are toxic to insects. By 2000, 89 different genes encoding crystal proteins had been cloned from B. thuringiensis strains (Crickmore, 2000; DeMaagd et al., 2001). This diversity, coupled with the narrow spectrum of activity of these proteins each toxin is active against a limited number of insect families has led to the extensive use of Bt as a biological insecticide and its increasing use in bio-engineering. Indeed, the last 10 years have seen a steady increase in the number of genetically modified crops producing Bt toxins (Navon, 2000). The total area under transgenic crops world-wide in 2002 was estimated at more than 60 million ha, with c. 14million ha (23%) under transgenic crops producing Bt toxins (Bt crops; James, 2002). Increases in sales of these Bt crops have increased the risk that the targeted insect pest species will become resistant to this ecologically valuable class of toxin (Gould, 1998; Wolfenbarger & Phifer, 2000). If transgenic crops are to be sustainable, a detailed understanding of the populations of target insects must be developed (Gould, 1998). However, the information required to develop ways of using transgenic insecticidal cultivars so as to avoid the rapid genetic adaptation of target pests is often unavailable. Comins (1977) was the first to show that random gene exchange between selected and unselected (referred as to refuge populations) insect populations in a patchwork can delay the evolution of resistance. This approach, coupled with the production of high doses of toxin by transgenic crops, has been referred to as the high dose/refuge strategy and appeared to be one of the best strategies of resistance management for transgenic Bt crops (Alstad & Andow, 1995; Vacher et al., 2003, 2004; Tabashnik et al., 2004). In this strategy, refuges are defined as habitats in which the target pest is not under selection pressure due to the toxin. These refuges correspond to all plants (crops or wild plants) that do not produce the Bt toxin but do provide a sustainable habitat for the development of the pest. The principle underlying the high dose/refuge strategy is that any resistant insects emerging from Bt crops are more likely to mate with one of the much larger number of susceptible pest insects emerging from the refuges than with each other, thereby decreasing the selection of Bt resistance alleles. An effective high dose/refuge strategy requires three main components. First, the increase in fitness conferred by resistance alleles must be recessive so that individuals heterozygous for a resistance allele are killed by the toxin produced by plant tissues. Second, resistance alleles must be rare so that few homozygotes survive on Bt crops. Third, one of the assumptions of the high dose/refuge strategy is that resistant insects selected on Bt crops mate randomly, or preferentially with susceptible insects preserved on non-Bt crops. The most important Bt crop world-wide is Bt maize, which covered c. 10million ha in 2002, equivalent to 80% of the total area under transgenic Bt crops. It has been grown in five countries: the U.S.A., Canada, Argentina, South Africa and Spain (James, 2002). The current Bt maize produces toxins Cry1Ab or Cry1F. These proteins are active against the European corn borer, Ostrinia nubilalis (Hubner), the major lepidopteran pest of maize in North America and Europe (Krattiger, 1997). Is it possible to Correspondence: Denis Bourguet, Centre de Biologie et de Gestion des Populations (CBGP), INRA Montpellier, Campus International de Baillarguet, CS 30 016, 34 988 Montferrier/Lez, France. Tel.: þ33 499623 366; fax: þ33 499623 345; e-mail: bourguet@ensam.inra.fr Physiological Entomology (2004) 29, 251–256