Analysis of the dynamics of adaptation to transgenic corn and crop rotation by western corn rootworm (Coleoptera: Chrysomelidae) using a daily time-step model

Western corn rootworm, Diabrotica virgifera virgifera LeConte, has overcome crop rotation in several areas of the north central United States. The effectiveness of crop rotation for management of corn rootworm has begun to fail in many areas of the midwestern United States, thus new management strategies need to be developed to control rotation-resistant populations. Transgenic corn, Zea mays L., effective against western corn rootworm, may be the most effective new technology for control of this pest in areas with or without populations adapted to crop rotation. We expanded a simulation model of the population dynamics and genetics of the western corn rootworm for a landscape of corn; soybean, Glycine max (L.); and other crops to study the simultaneous development of resistance to both crop rotation and transgenic corn. Results indicate that planting transgenic corn to first-year cornfields is a robust strategy to prevent resistance to both crop rotation and transgenic corn in areas where rotation-resistant populations are currently a problem or may be a problem in the future. In these areas, planting transgenic corn only in continuous cornfields is not an effective strategy to prevent resistance to either trait. In areas without rotation-resistant populations, gene expression of the allele for resistance to transgenic corn, R, is the most important factor affecting the evolution of resistance. If R is recessive, resistance can be delayed longer than 15 yr. If R is dominant, resistance may be difficult to prevent. In a sensitivity analysis, results indicate that density dependence, rotational level in the landscape, and initial allele frequency are the three most important factors affecting the results.     

Western corn rootworm (Coleoptera: Chrysomelidae) dispersal and adaptation to single-toxin transgenic corn deployed with block or blended refuge

A simulation model of the temporal and spatial dynamics and population genetics of western corn rootworm, Diabrotica virgifera virgifera LeConte, was created to evaluate the use of block refuges and seed blends in the management of resistance to transgenic insecticidal corn (Zea mays L.). This Bt corn expresses one transgenic corn event, DAS-59122-7, that produces a binary insecticidal protein toxin (Cry34Ab1/Cry35Ab1) and provides host-plant resistance. The model incorporates the latest information about larval and adult behavior. Results of this modeling effort indicate that the seed-blend scenarios in many cases produced equal or greater durability than block refuges that were relocated each year. Resistance evolved in the most likely scenarios in 10-16 yr. Our standard analysis presumed complete adoption of 59122 corn by all farmers in our hypothetical region, no crop rotation, and 100% compliance with Insect Resistant Management (IRM) regulations. As compliance levels declined, resistance evolved faster when block refuges were deployed. Seed treatments that killed the pest when applied to all seeds in a seed blend or just to seeds in Bt corn blocks delayed evolution of resistance. Greater control of the pest population by the seed treatment facilitated longer durability of the transgenic trait. Therefore, data support the concept that pyramiding a transgenic insecticidal trait with a highly efficacious insecticidal seed treatment can delay evolution of resistance.     

Using a generational time-step model to simulate dynamics of adaptation to transgenic corn and crop rotation by western corn rootworm (Coleoptera: Chrysomelidae)

We expanded a simulation model of the population dynamics and genetics of the western corn rootworm for a landscape of corn, soybean, and other crops to study the simultaneous development of resistance to both crop rotation and transgenic corn. Transgenic corn effective against corn rootworm was recently approved in 2003 and may be a very effective new technology for control of western corn rootworm in areas with or without the rotation-resistant variant. In simulations of areas with rotation-resistant populations, planting transgenic corn to only rotated cornfields was a robust strategy to prevent resistance to both traits. In these areas, planting transgenic corn to only continuous fields was not an effective strategy for preventing adaptation to crop rotation or transgenic corn. In areas without rotation-resistant phenotypes, gene expression of the allele for resistance to transgenic corn was the most important factor affecting the development of resistance to transgenic corn. If the allele for resistance to transgenic corn is recessive, resistance can be delayed longer than 15 yr, but if the resistant allele is dominant then resistance usually developed within 15 yr. In a sensitivity analysis, among the parameters investigated, initial allele frequency and density dependence were the two most important factors affecting the evolution of resistance. We compared the results of this simulation model with a more complicated model and results between the two were similar. This indicates that results from a simpler model with a generational time-step can compare favorably with a more complex model with a daily time-step.     

Economic analysis of dynamic management strategies utilizing. Transgenic corn for control of western corn rootworm (Coleoptera: Chrysomelidae)

We studied management strategies for western corn rootworm, Diabrotica virgifera virgifera LeConte, using transgenic corn, Zea mays L., from both a biological and an economic perspective. In areas with and without populations adapted to a 2-yr rotation of corn and soybean (rotation-resistant), the standard management strategy was to plant 80% of a cornfield (rotated and continuous) to a transgenic cultivar each year. In each area, we also studied dynamic management strategies where the proportion of transgenic corn increased over time in a region. We also analyzed management strategies for a single field that is the first to adopt transgenic corn within a larger unmanaged region. In all areas, increasing the expression of the toxin in the plant increased economic returns. In areas without rotation-resistance, planting 80% transgenic corn in the continuous cornfield each year generated the greatest returns with a medium toxin dose or greater. In areas with alleles for rotation-resistance at low initial levels, a 2-yr rotation of nontransgenic corn and soybean, Glycine max (L.) Merr., may be the most economical strategy if resistance to crop rotation is recessive. If resistance to crop rotation is additive or dominant, planting transgenic corn in the rotated cornfield was the most effective strategy. In areas where rotation-resistance is already a severe problem, planting transgenic corn in the rotated cornfield each year was always the most economical strategy. In some cases the strategies that increased the proportion of transgenic corn in the region over time increased returns compared with the standard strategies. With these strategies the evolution of resistance to crop rotation occurred more rapidly but resistance to transgenic corn was delayed compared with the standard management strategy. In areas not managed by a regional norm, increasing the proportion of transgenic corn and increasing toxin dose in the managed field generally increased returns. In a sensitivity analysis, among the parameters investigated, only density-dependent survival affected the results.     

Modeling larval survival and movement to evaluate seed mixtures of transgenic corn for control of western corn rootworm (Coleoptera: Chrysomelidae)

I expanded the population dynamics and genetics model published in 2005 by Crowder and Onstad to include larval survival and movement to evaluate the role of mixtures of transgenic and nontransgenic corn, Zea mays L., seed for resistance management of western corn rootworm. I studied both density-independent and density-dependent toxin survival. In all but the worst-case scenarios, resistance did not evolve within 30 yr when the resistance allele, R, was recessive. The standard model with density-independent toxin survival based on the expression of a medium dose of toxin indicated that 50% R allele frequency will be reached by years 5 and 7, respectively, with dominant and partially recessive expression and 20% nontransgenic seed. The standard model with density-dependent toxin survival indicates that resistance will occur in year 5 under the same conditions. These results are similar to the published results of Crowder and Onstad who studied a model with adjacent block refuges and mostly nonrandom mating in the landscape (random only within each block). Results depended on the heterozygote advantage (differential survival between SS and RS) and the degree of random mating provided by the seed mixture.     

Planting transgenic insecticidal corn based on economic thresholds: consequences for integrated pest management and insect resistance management

A simulation model of the western corn rootworm, Diabrotica virgifera virgifera LeConte, was used to investigate whether sampling and economic thresholds can improve integrated pest management (IPM) and insect resistance management (IRM) when transgenic insecticidal crops are used for insect pest management. When transgenic corn killed at least 80% of susceptible larvae, the calculated economic threshold increased linearly as the proportion of susceptible beetles surviving the toxin increased. The use of economic thresholds slightly slowed the evolution of resistance to transgenic insecticidal crops. In areas with or without rotation-resistant western corn rootworm phenotypes, the use of sampling and economic thresholds generated similar returns compared with strategies of planting transgenic corn, Zea mays L., every season. Because transgenic crops are extremely effective, farmers may be inclined to plant transgenic crops every season rather than implementing costly and time-consuming sampling protocols.     

Economics versus alleles: balancing integrated pest management and insect resistance management for rotation-resistant western corn rootworm (Coleoptera: Chrysomelidae)

Western corn rootworm, Diabrotica virgifera virgifera LeConte, has overcome crop rotation in several areas of the central United States. We expanded a simple model of adult behavior and population genetics to explain how rotation resistance may have developed and to study ways to manage the western corn rootworm in a landscape of corn, soybean, and winter wheat where evolution of resistance may occur. We modeled six alternative management strategies over a 15-yr time horizon, as well as a strategy involving a 2-yr rotation of corn and soybean in 85% of the landscape, to investigate their effectiveness from both a biological and economic perspective. Generally, resistance to crop rotation evolves in fewer than 15 yr, and the rate of evolution increases as the level of rotated landscape (selection pressure) increases. When resistance is recessive, all six alternative strategies were effective at preventing evolution of rotation resistance. The two most successful strategies were the use of transgenic rotated corn in a 2-yr rotation and a 3-yr rotation of corn, soybean, and wheat with unattractive wheat (for oviposition) preceding corn. Results were most sensitive to increases in the initial allele frequency and modifications of the density-dependent survival function. Economically, three alternative strategies were robust solutions to the problem, if technology fees were not too high. Repellant soybean, attractive rotated corn, and transgenic rotated corn, all in 2-yr rotations, were economically valuable approaches. However, even the currently common 2-yr rotation was economical when resistance was recessive and the actual costs of resistance would not be paid until far in the future.     

Evaluation of oviposition deterrence in management of resistance to transgenic corn by European corn borer (Lepidoptera: Crambidae)

We modified an existing model for European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae), population dynamics and genetics to evaluate the effectiveness of oviposition deterrence in transgenic fields for resistance management. We simulated two types of deterrence: one type has females reducing their oviposition because of lost opportunities to lay eggs (eggs lost), and the other type has the deterred females moving to the refuge to lay eggs. Oviposition deterrence was clearly effective in extending the time to resistance to transgenic corn (R allele) in the European corn borer, particularly when 80% or more of the eggs were deterred from being oviposited on the transgenic plants. With 90% of eggs deterred, the time required to reach 50% R-allele frequency increases 3.7- to 5.5-fold compared with the no-deterrence scenario. The time to 50% R-allele frequency was similar for the two types of simulated deterrence, but the densities of the European corn borer were 100-fold higher when the deterred females oviposited in the refuge. The Y allele for insensitivity or resistance to deterrence never reached 50% within the 50-yr time line for these simulations except when the R allele was dominant and the Y allele was not recessive. The time to 50% Y-allele frequency was 33 and 26 yr when the Y allele was additive or dominant, respectively, when 50% of the eggs were deterred, but the time decreased to 18 and 16 yr when 90% of the eggs were deterred. The effectiveness of oviposition deterrence on time to resistance to transgenic insecticidal plants was not changed much when we altered our assumptions about behavior in a sensitivity analysis.     

Delaying corn rootworm resistance to Bt corn

Transgenic crops producing Bacillus thuringiensis (Bt) toxins for insect control have been successful, but their efficacy is reduced when pests evolve resistance. To delay pest resistance to Bt crops, the U.S. Environmental Protection Agency (EPA) has required refuges of host plants that do not produce Bt toxins to promote survival of susceptible pests. Such refuges are expected to be most effective if the Bt plants deliver a dose of toxin high enough to kill nearly all hybrid progeny produced by matings between resistant and susceptible pests. In 2003, the EPA first registered corn, Zea mays L., producing a Bt toxin (Cry3Bb1) that kills western corn rootworm, Diabrotica virgifera virgifera LeConte, one of the most economically important crop pests in the United States. The EPA requires minimum refuges of 20% for Cry3Bb1 corn and 5% for corn producing two Bt toxins active against corn rootworms. We conclude that the current refuge requirements are not adequate, because Bt corn hybrids active against corn rootworms do not meet the high-dose standard, and western corn rootworm has rapidly evolved resistance to Cry3Bb1 corn in the laboratory, greenhouse, and field. Accordingly, we recommend increasing the minimum refuge for Bt corn targeting corn rootworms to 50% for plants producing one toxin active against these pests and to 20% for plants producing two toxins active against these pests. Increasing the minimum refuge percentage can help to delay pest resistance, encourage integrated pest management, and promote more sustainable crop protection.     

Post-establishment movement of western corn rootworm larvae (Coleoptera: Chrysomelidae) in Central Missouri corn

If registered, transgenic corn, Zea mays L., with corn rootworm resistance will offer a viable alternative to insecticides for managing Diabrotica spp. corn rootworms. Resistance management to maintain susceptibility is in the interest of growers, the Environmental Protection Agency, and industry, but little is known about many aspects of corn rootworm biology required for an effective resistance management program. The extent of larval movement by the western corn rootworm, Diabrotica virgifera virgifera LeConte, that occurs from plant-to-plant or row-to-row after initial establishment was evaluated in 1998 and 1999 in a Central Missouri cornfield. Post-establishment movement by western corn rootworm larvae was clearly documented in two of four treatment combinations in 1999 where larvae moved up to three plants down the row and across a 0.46-m row. Larvae did not significantly cross a 0.91-m row after initial host establishment in 1998 or 1999, whether or not the soil had been compacted by a tractor and planter. In the current experiment, western corn rootworm larvae moved from highly damaged, infested plants to nearby plants with little to no previous root damage. Our data do not provide significant insight into how larvae might disperse after initial establishment when all plants in an area are heavily damaged or when only moderate damage occurs on an infested plant. A similar situation might also occur if a seed mixture of transgenic and isoline plants were used and if transgenic plants with rootworm resistance are not repellent to corn rootworm larvae.