The global area planted to Bt crops covered over 66 million hectares in 2011. Insect resistance management (IRM) is implemented to protect the efficacy of commercial transgenic crops expressing Bacillus thuringiensis toxins because the benefits of the pest susceptibility to Bt toxins is considered as a common good. Simulation models have helped guide the USEPA’s regulatory decisions on the IRM requirements of both Bt cotton and Bt corn plant-incorporated protectants (PIPs) since the late 1990s. For my dissertation research, I built four species-specific, simulation models to study the evolution of resistance by four insect pests of corn or cowpea to transgenic crops to 1) forecast the durability of traits in transgenic crops, 2) study the effects of biological, ecological factors on resistance evolution, 3) investigate potential concerns in the use of transgenic cowpea for controlling an insect pest of stored products, and 4) provide simulation models for future research in IRM.A mathematical model with processes reflecting larval mortality resulting from feeding on cross-pollinated ears or Bt ears of corn was used to analyze the risk of evolution of Cry-toxin resistance in Ostrinia nubilalis. In the simulations, evolution of resistance was delayed equally well by both seed-blend and block refuges with the same proportion of refuge. The results showed that Bt-pollen drift has little impact on the evolution of Bt resistance in O. nubilalis. However, low-toxin expression in ears of transgenic corn can reduce the durability of transgenic corn expressing single toxin, while durability of pyramided corn hybrids is not significantly reduced. The toxin-survival rate of heterozygous larvae in Bt-corn ears expressing one or two proteins has more impact on evolution of Bt resistance in O. nubilalis than the parameters related to larval movement to Bt ears or the toxin-survival rate of the homozygous susceptible larvae in Bt ears. Bt resistance evolves slower when toxin mortality is distributed across the first two larval stadia than when only the first instars are susceptible to Bt toxins. The study suggested that stakeholders should examine toxin-survival rates for insect pests and take into account that instars may feed on different parts of Bt corn.An emergence delay and female-skewed-sex-ratios among adults of Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) from Bt corn have been reported in field studies. A simulation model was used to study the effect of a maturation delay and a female-skewed-sex-ratio for D. v. virgifera emerging from Bt corn on the evolution of Bt resistance. Early emergence of resistant beetles from Bt corn accelerates evolution of Bt-resistance; however, an emergence delay among resistant beetles from Bt corn slows resistance evolution.A shift in the time of emergence for homozygous-susceptible beetles from Bt corn does not have a significant effect on the evolution of Bt-resistance in D. v. virgifera. Resistance to Bt evolves faster when males are more susceptible to Bt toxins than females. This simulation study suggested that an emergence delay for beetles in Bt corn is not a major concern for managing resistance by D. v. virgifera to single-toxin or pyramided-Bt corn.The cowpea weevil, Callosobruchus maculatus F. (Coleoptera: Bruchidae), can cause up to 100% yield loss of stored cowpea seeds, Vigna unguiculata (L.) Walp, in a few months in West Africa. Genes expressing toxins delaying insect maturation (MDTs) are available for genetic engineering. A simulation model was used to investigate the possibility of the use of MDTs to manage C. maculatus. Specifically, I studied the effect of transgenic cowpea expressing a MDT, an insecticide, or both, on the evolution of resistance by C. maculatus at constant temperature. Transgenic cowpea expressing a non-lethal MDT causing 50% maturation delay did not prevent 98% yield loss by C. maculatus for one year. Transgenic cowpea expressing a lethal MDT causing 50% maturation delay and 90% mortality protected 80% of yield for one year at 25°C, but its durability was only three years. Mortality caused by a maturation delay improves the efficacy of transgenic cowpea expressing only a lethal MDT, but significantly reduces the durability of transgenic cowpea if the heterozygotes at the locus controlling resistance to a lethal MDT survive more than the homozygous susceptible individuals. I concluded that transgenic cowpea expressing only a MDT has little value for managing C. maculatus. The resistance by C. maculatus to transgenic cowpea expressing only an insecticide rapidly evolves. Stacking a gene expressing a non-lethal MDT and a gene expressing an insecticide in transgenic cowpea did not significantly improve the durability of an insecticide, but stacking a gene expressing a lethal MDT and a gene expressing an insecticide in transgenic cowpea significantly improved the durability of an insecticide and a MDT.Major resistance alleles to Cry1Ab corn in the sugarcane borer, Diatraea saccharalis (F.) (Lepidoptera: Crambidae), were first detected in a field population in northeast Louisiana in 2004, and the estimated frequency of the resistance allele was 0.0177 in populations in Louisiana in 2009. I used a demographic model to study the evolution of resistance by D. saccharalis to transgenic corn expressing one or two Bt proteins. The effects of biological and agricultural factors on resistance evolution were studied by using sensitivity analyses to improve insect resistance management strategies for D. saccharalis. An increase in the proportion of refuge did not always improve the durability of Bt corn if there were sugarcane, sorghum, or rice in the agro-ecosystem. The evolution of Bt-resistance accelerated when larvae entered diapause for overwintering early. A low frequency of inter-field movement of moths delayed the evolution of resistance to single-protein or pyramided-Bt corn when the proportion of refuge was 20%, but it accelerated Bt-resistance evolution when the proportion of refuge was 50%.My modeling studies focused on preventative IRM programs for major insect pests of corn or cowpea, and identified challenges in managing insect resistance to transgenic crops. The three major challenges were 1) low susceptibility of insect pests to Bt toxins expressed in single-toxin-Bt corn, 2) lack of alternative IRM strategies, and 3) lack of knowledge about the biology and behavior of an insect pest.Complexity in designing IRM strategies has increased as the number of plant-incorporated protectants (PIPs) targeting insect pests in the field has increased. IRM programs need to adapt to changes in Bt crop technology and be based on an understanding of the factors influencing the evolution of resistance. Over the past 15 years, EPA has made changes to the IRM requirements of Bt PIP products and the regulatory policy to strengthen the refuge requirements, resistance monitoring, and compliance assurance programs. The challenge for a risk manager is how to balance the need to maintain the pest susceptibility, the cost of compliance with IRM requirements, willingness of the growers to comply with the IRM requirements, and environmental benefits. The economics of the crop production system should be considered for IRM strategies over a long term. Thus, IRM and integrated pest management (IPM) should be considered together because robust IRM strategies are complemented by good IPM. Implementing principles of IPM will reduce unnecessary exposure of PIPs in insects, which will improve the management of the pest susceptibility to PIPs.
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Modeling insect resistance to transgenic corn and cowpea
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