Modeling evolution of resistance of sugarcane borer (Lepidoptera: Crambidae) to transgenic Bt corn.

Diatraea saccharalis (F.) (Lepidoptera: Crambidae) is a target pest of transgenic corn expressing Bacillus thuringiensis (Bt) protein, and the first evidence of resistance by D. saccharalis to Cry1Ab corn was detected in a field population in northeast Louisiana in 2004. We used a model of population dynamics and genetics of D. saccharalis to 1) study the effect of interfield dispersal, the first date that larvae enter diapause for overwintering, toxin mortality, the proportion of non-Bt corn in the corn patch, and the area of a crop patch on Bt resistance evolution; and 2) to identify gaps in empirical knowledge for managing D. saccharalis resistance to Bt corn. Increasing, the proportion of corn refuge did not always improve the durability of Bt corn if the landscape also contained sugarcane, sorghum, or rice. In the landscape, which consisted of 90% corn area, 5% sorghum area, and 5% rice area, the durability of single-protein Bt corn was 40 yr when the proportion of corn refuge was 0.2 but 16 yr when the proportion of corn refuge was 0.5. The Bt resistance evolution was sensitive to a change (from Julian date 260 to 272) in the first date larvae enter diapause for overwintering and moth movement. In the landscapes with Bt corn, non-Bt corn, sugarcane, sorghum, and rice, the evolution of Bt resistance accelerated when larvae entered diapause for overwintering early. Intermediate rates of moth movement delayed evolution of resistance more than either extremely low or high rates. This study suggested that heterogeneity in the agrolandscapes may complicate the strategy for managing Bt resistance in D. saccharalis, and designing a Bt resistance management strategy for D. saccharalis is challenging because of a lack of empirical data about overwintering and moth movement.

Modeling evolution of resistance by Maruca vitrata (Lepidoptera: Crambidae) to transgenic insecticidal cowpea in Africa.

We created a detailed model of the Maruca vitrata (F.) and cowpea [Vigna unguiculata (L.) Walp] system to study the possible evolution of resistance by the insect to transgenic insecticidal cowpea, which is under development. We focused on population dynamics and genetics in a region of west Africa. We simulated single-toxin and pyramided (two-toxin) cowpea and emphasized conservative, worst-case scenarios in our analysis. The results indicate that as long as a pyramided, transgenic cowpea can be developed, seed saving by farmers and reliance on natural refuge are not major problems for resistance management. Furthermore, it is possible that one or both toxins in the pyramid may not need to be high dose for evolution to be delayed significantly (>20 yr or 80 generations for resistance to become a concern if transgenic cowpea is deployed in areas where M. vitrata is endemic). If efforts are made to deploy transgenic cowpea only into the regions where M. vitrata is not endemic, then there is little to no concern with resistance emerging in the M. vitrata population.

Modeling the impact of cross-pollination and low toxin expression in corn kernels on adaptation of European corn borer (Lepidoptera: Crambidae) to transgenic insecticidal corn.

We used a mathematical model with processes reflecting larval mortality resulting from feeding on cross-pollinated ears or Bt ears of corn to analyze the risk of evolution of Cry-toxin resistance in Ostrinia nubilalis (Hübner). In the simulations, evolution of resistance was delayed equally well by both seed mixtures and blocks with the same proportion of refuge. Our 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, whereas 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. We suggest that stakeholders examine toxin-survival rates for insect pests and take into account that instars may feed on different parts of Bt corn.

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.

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.

Forecasting seasonal population growth of Aphis glycines (Hemiptera: Aphididae) in soybean in Illinois.

From 2001 to 2004, 252 fifty-plant samples were collected from commercial soybean, Glycine max L., fields in three townships (93-km2 area) in Illinois. Townships were sampled every 3 wk from late June or early July when aphids (Aphis glycines Matsumura) first invaded the townships to early August. We used linear regression of 18 mean township field densities to calibrate several simple models to predict the change in aphid population density in a township from one sampling date to the next. The best exponential model for the complete data set has an r2 = 0.54, Y2 = Ylexp (0.09659 x DAY), where Y1 and Y2 are the first and second samples of aphids separated by a 3-wk period (the number of days, DAY). Our intrinsic rate of increase for the population is much lower than rates calculated in other studies. The best single-variable linear model has an r2 = 0.88, Y2 = Y1 + 0.1084 x Y1 x DAY. The latter model indicates the value of including monitoring data in the prediction. The best two-variable model has an R2 = 0.98, Y2 = Y1 + 0.08136 x Y1 x DAY + 0.000080 x N1(2) x DAY, where N1(2) x DAY is the interaction term for initial, squared, sample density of the season multiplied by the number of days between samples. The latter two models indicate that the change in the population density is greater for more dense populations. Degree-days were generally inferior to days as the time component in the simple models.

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.

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.

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.

Effect of extended diapause on evolution of resistance to transgenic Bacillus thuringiensis corn by northern corn rootworm (Coleoptera: Chrysomelidae).

We develop a population genetics model for the northern corn rootworm, Diabrotica barberi Smith & Lawrence, to examine the effect of extended diapause on the evolution of resistance to transgenic Bacillus thuringiensis (Bt) corn, Zea mays L. We model conditions found in the center of the extended diapause problem along the Minnesota-South Dakota-Iowa borders. The proportion of resistance alleles in eggs oviposited after 15 simulated years is used to measure the evolution of resistance. Sensitivity analysis indicates that although population genetics parameters (fecundity, initial egg density, density-dependent larval survival, random mating, insecticide mortality, and gene expression) affect the evolution of resistance, product characteristics (e.g., Bt toxin dose) and farmer management practices (e.g., insecticide use on refuge corn and rotation pattern) generally have a larger impact on the development of resistance. Exceptions to this generalization exist: 1) if the resistance allele is dominant, resistance evolves quickly; 2) the level of random mating is an important determinant of how quickly resistance evolves for a theoretical high dose product; and 3) small differences in insecticide mortality imply large differences in resistance for medium- and low-dose products with high levels of Bt corn adoption and a predominance of 1- and 2-yr corn rotations. When extended diapause spreads into a new area, it typically reduces resistance to Bt corn, assuming Bt corn is used only on continuous corn. In the study region where extended diapause already exists, increasing extended diapause (increasing hatch rates after two or three winters while holding total hatch constant), tends to increase resistance because the resistance increasing effect of the hatch rate after two winters dominates the resistance decreasing effect of the hatch rate after three winters. However, this is not always the case, because combinations of rotation pattern, toxin dose, and soil insecticide use exist for which the net effect of extended diapause decreases resistance. Results are interpreted as a combination of two offsetting effects. First, extended diapause injects older alleles with lower resistance allele frequencies into the breeding population, which slows resistance. Second, extended diapause speeds the population's recovery from perturbations (reduces the undercompensating density dependence of population dynamics), which accelerates resistance.

Description and analysis of two internet-based databases of insect pathogens: EDWIP and VIDIL.

In 1996, two searchable databases covering insect pathogens were posted on the World Wide Web: the Ecological Database of the World's Insect Pathogens (EDWIP) and the Viral Diseases of Insects in the Literature database (VIDIL). In this paper, we describe the format and contents of EDWIP and VIDIL on the World Wide Web. EDWIP contains over 9,400 pathogen-host association records, 677 negative test result or "no association" records, 4,454 host species, 2,285 pathogen species records, and 2,057 bibliographical references. Species of Coleoptera and Lepidoptera are the best represented groups in EDWIP. Lepidopteran species account for the most associations of any host order in EDWIP, over 2,500, or 27%. Of the pathogen groups, Protozoa (including microsporidia) accounted for nearly 66% of the pathogen species records and over 40% of the association records in EDWIP. Fungi account for only 18% of the pathogen species, but nearly 33% of the association records. Habitats dominated by human activities (e.g., crop, stored product, and human dwelling) account for most of the host habitats recorded in EDWIP. The United States and Japan are the most common locations and the Nearctic and Palearctic are the most common biogeographic regions reported in EDWIP. There are 4,801 annotated bibliographic records in VIDIL.

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.

Modeling the development of resistance by stalk-boring lepidopteran insects (Crambidae) in areas with transgenic corn and frequent insecticide use.

We simulated the population dynamics and population genetics of two bivoltine species of corn borers, the European corn borer, Ostrinia nubilalis (Hübner), and the southwestern corn borer, Diatraea grandiosella Dyar, in a hypothetical region of irrigated transgenic and nontransgenic corn where insecticide was applied only to the nontransgenic refuge crop. Over the 100-yr time horizon, resistance developed quickly in both species and to both transgenic corn and the insecticide when the allele for resistance to the respective toxin was dominant. When the allele for transgenic resistance was not dominant and the refuge location was constant over the time horizon, spraying the refuge to control southwestern corn borer had no effect on how quickly resistance to the transgenic corn developed. In contrast, the European corn borer developed resistance to transgenic corn much sooner when the refuge was sprayed once per year, and the time to 3% resistance allele frequency decreased as efficacy of the insecticide increased. Only when the refuge was treated less than once every 5 yr (10 generations) did the frequency of application decline enough to permit resistance management for the European corn borer to approximate the effectiveness of an unsprayed refuge. A consistently sprayed refuge <40% of the corn acreage was an inadequate resistance management strategy for the European corn borer even when a low efficacy insecticide (70% mortality) was used. When assumptions about European corn borer adult behavior were changed and the adults behaved similarly to adult southwestern corn borer, the development of resistance to the transgenic crop was slowed significantly.

Modeling the dynamics of adaptation to transgenic corn by western corn rootworm (Coleoptera: Chrysomelidae).

A simulation model of the population dynamics and genetics of the western corn rootworm, Diabrotica virgifera virgifera LeConte, was created for a landscape of corn, soybean, and other crops. Although the model was created to study a 2-locus problem for beetles having genes for resistance to both crop rotation and transgenic corn, during this first phase of the project, the model was simulated to evaluate only resistance management plans for transgenic corn. Allele expression in the rootworm and toxin dose in the corn plant were the two most important factors affecting resistance development. A dominant resistance allele allowed quick evolution of resistance to transgenic corn, whereas a recessive allele delayed resistance >99 yr. With high dosages of toxin and additive expression, the time required to reach 3% resistance allele frequency ranged from 13 to >99 yr. With additive expression, lower dosages permitted the resistant allele frequency to reach 3% in 2-9 yr with refuges occupying 5-30% of the land. The results were sensitive to delays in emergence by susceptible adults and configuration of the refuge (row strips versus blocks).

Seed mixtures as a resistance management strategy for European corn borers (Lepidoptera: Crambidae) infesting transgenic corn expressing Cry1Ab protein.

Dispersal of neonate European corn borers, Ostrinia nubilalis (Hübner), in seed mixtures of transgenic corn expressing Cry1Ab protein (Bt+) and nontransgenic corn (Bt-) was evaluated in a 2-yr field study. The main objective was to determine if larval dispersal limits the effectiveness of seed mixtures as a resistance management strategy. Mixtures evaluated included (1) all Bt+ plants, (2) every fifth plant Bt- with remaining plants Bt+, (3) every fifth plant Bt+ with remaining plants Bt-, and (4) all Bt- plants. The transformation events MON 802 (B73 BC1F2 x Mol7) and MON 810 (B73 BC1F1 x Mo17), which express the Cry1Ab endotoxin isolated from Bacillus thuringiensis subsp. kurstaki, were used as the sources of Bt+ seed in 1994 and 1995, respectively (YieldGard, Monsanto, St. Louis, MO). At corn growth stage V6-V8, subplots within each mixture (15-20 plants each) were infested so that every fifth plant in mixtures 1 and 4, every Bt- plant in mixture 2, and every Bt+ plant in mixture 3 received two egg masses. Larval sampling over a 21-d period indicated increased neonate dispersal off of Bt+ plants, reduced survival of larvae that dispersed from Bt+ plants to Bt- plants, and a low incidence of late-instar movement from Bt- plants to Bt+ plants. Computer simulations based on mortality and dispersal estimates from this study indicate that seed mixtures will delay the evolution of resistant European corn borer populations compared with uniform planting of transgenic corn. However, resistant European corn borer populations likely will develop faster in seed mixes compared with separate plantings of Bt and non-Bt corn.

Temporal and spatial scales in epidemiological concepts.

Traditional concepts in epidemiology are reviewed from ecological, cultural, and logical perspectives. In zoological epidemiology (including the study of human and livestock diseases caused by pathogens), temporal and spatial scales are typically not used in definitions, by hypotheses, and theories concerning epidemic and endemic diseases. The same is true for botanical and theoretical epidemiology, although these two subdisciplines use a different definition of an epidemic than does zoological epidemiology. If hypotheses are to be tested and implemented, more precise concepts that include general temporal and spatial scales are needed. Criteria proposed here for identifying temporal and spatial scales are based on the need for consistency of observation and ecological validity. Consistency of observation depends upon the relative life cycles of the hosts and pathogens and upon the environmental effects that lead to stable or unstable population structures. Pathogens are classified as absent, sporadic, or persistent (endemic). Epidemics can occur in the latter two cases but require a separate evaluation. A definition of an epidemic based on temporal and spatial scales and statistics is proposed for use by all subdisciplines. An epidemic occurs when an indicator variable reaches a statistically unusually high value due to transmission of a pathogen in an ecologically proper space-time unit. Threshold theorems in botanical and theoretical epidemiology are also discussed. These proposals do not directly affect modeling, but changes to hypotheses may influence model analyses.