Heritability and stability of resistance to Bacillus thuringiensis in Ostrinia nubilalis (Lepidoptera: Pyralidae)
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1 Bulletin of Entomological Research (1999) 89, Heritability and stability of resistance to Bacillus thuringiensis in Ostrinia nubilalis (Lepidoptera: Pyralidae) F. Huang 1, R.A. Higgins 1 *, and L.L. Buschman 2 1 Department of Entomology, 123 Waters Hall, Kansas State University, Manhattan, Kansas 66506, USA: 2 Kansas State University Southwest Research-Extension Center, 4500 East Mary Street, Garden City, Kansas 67846, USA Abstract Realized heritability, h 2, of resistance in European corn borer, Ostrinia nubilalis (Hübner), to Bacillus thuringiensis Berliner ssp. kurstaki endotoxins was examined in five resistant laboratory colonies. These colonies were reared on a meridic diet that incorporated a commercial formulation of B. thuringiensis, Dipel ES. Resistance in these colonies reached by the seventh to twentieth selected generations and then plateaued. The realized heritability of resistance averaged over all selected generations for the five colonies. In the three Iowa colonies, the highest realized heritability, , occurred during the second period of selection (seventh to thirteenth selected generations). In the two Kansas colonies, the highest realized heritability, 0.36 and 0.46, occurred during the first period of selection (first to sixth selected generations). In the absence of selection pressure, resistance in the southwest Kansas colony decreased from 62 to 42 after two generations, and remained at about that level for the next five generations. Introduction ÔRealized heritabilityõ, h 2, the proportion of phenotypic variation accounted for by additive genetic variation, is a parameter that can be calculated to estimate the time required for changes to occur in gene frequency under different selection scenarios (Tabashnik, 1992). Estimation of heritability can also facilitate comparisons among different selection experiments (Falconer, 1981; Firko & Hayes, 1990; Tabashnik, 1992; Omer et al., 1993; Tabashnik & McGaughey, 1994), with no assumptions beyond those used in probit analysis (Tabashnik, 1992). In addition, there are no assumptions about the mode of inheritance so it can be used whether one or many genes control resistance (Tanaka & Noppun, 1989; Firko & Hayes, 1990; Tabashnik, 1992, 1994). Since 1994, five colonies of European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), have been selected with a commercial formulation of Bacillus *Author for correspondence Fax: rhiggins@oz.oznet.ksu.edu thuringiensis Berliner ssp. kurstaki to study changes in their susceptibility to B. thuringiensis endotoxins. The susceptibility of these colonies decreased over six to 14 selected generations (Huang et al., 1997). This paper reports the results of continued selection of the five O. nubilalis colonies and calculates the realized heritability, h 2, for these colonies. It also reports the results of an evaluation of the stability of the resistance in the absence of selection pressure in the most resistant of the five O. nubilalis colonies. Materials and methods Insect strains, selections, and bioassays Three Iowa colonies, IA-1, IA-2, and IA-3, of O. nubilalis were initiated using egg masses provided by the USDA Corn Insects Laboratory at Ames, Iowa, in 1994 and The IA-1 colony was initiated in 1994 with about 500 egg masses from a colony that had been started from insects collected from fields in central Iowa in This colony was in the sixth cultured generation when selection started. The IA-2 and IA-3 colonies were started in 1995 with about 4000 and 3000 egg
2 450 F. Huang et al. masses, respectively, from a colony that had been started from insects collected from fields in central Iowa in This colony was in the fourth generation in culture when selection started. The KS-NE colony was established with 125 egg masses collected from fields near Manhattan in northeast Kansas in This colony was in the second generation in culture when selection started. The KS-SC colony was established with 48 egg masses collected from fields near St John, in south central Kansas in This colony was in the second generation in culture when selection started. An average O. nubilalis egg mass contains about 20 eggs. Our O. nubilalis culture and rearing methods were adapted from those used by the USDA Corn Insects Laboratory in Ames, Iowa (Guthrie et al., 1965; Reed et al., 1972; Ostlie et al., 1984). Larval susceptibility was determined in bioassays in which O. nubilalis larvae were placed on diets incorporating different concentrations of Dipel ES TM. Dipel ES is a commercial formulation of B. thuringiensis ssp. kurstaki (17,600 IU mg 1, Abbott, North Chicago, Illinois). Dipel contains Cry1Aa, Cry1Ab, Cry1Ac, Cry2A, and Cry2B endotoxins of B. thuringiensis. A control and six of the following dilutions were employed in each bioassay: 0.01, 0.03, 0.09, 0.27, 0.81, 2.43, 7.29, and ml Dipel kg 1 diet. Approximately 2 ml of prepared diet was poured into each cell of the 128-cell trays (Bio-Ba-128, C-D International Inc. Pitman, New Jersey). One neonate larva was placed in each cell. Larval mortality was assessed on the fifth day after inoculation. For each concentration, there were four replicates of 32 larvae. The bioassay trays were held in a growth chamber maintained at 27 C and a 24:0 L:D photoperiod (Huang et al., 1997). Selection for resistance in O. nubilalis to B. thuringiensis was conducted by incorporating Dipel into diets at dosages selected to produce 60 99% mortality. An unselected strain of each colony was maintained on untreated diet. The resistance factors (RF; LC 50 of selected strain divided by pooled LC 50 of the unselected control strain) were for the three Iowa colonies after nine to 14 selected generations, 35 for the colony from northeast Kansas (KS- NE) after six selected generations, and for the colony from south central Kansas (KS-SC) after five to seven selected generations (Huang et al., 1997). SAS probit analysis (SAS Institute, 1990) was used to calculate the LC 50, 95% confidence interval, and the slope. Control data for the Iowa strains were based on six bioassays of the first, second, eighteenth, and thirtieth generations of the unselected strain of the IA-1 colony and of the first generations of the IA-2 and IA-3 colonies. Control data for the KS-NE strain were based on four bioassays of the first, second, seventh, and fifteenth generations of the unselected strain of the KS-NE colony. Control data for the KS-SC strain were based on five bioassays of the first, second, seventh, ninth, and fifteenth generations of the unselected strain of the KS-SC colony. Analysis of realized heritability Data for analysing the realized heritability, h 2, of resistance of O. nubilalis to Dipel were the results reported in Huang et al. (1997) and the results from the continuing selection of the O. nubilalis colonies. We estimated the realized heritability of resistance using the method described by Tabashnik (1992): h 2 = R/S where R is the response to selection, the difference between the mean phenotype of the selected offspring and the parental generation before selection and S is the selection differential, the difference between the mean phenotype of the selected parents and the parental generation before selection (Falconer, 1981; Tabashnik & McGaughey, 1994). The realized heritability may change during the selection regime (Firko & Hayes, 1990), therefore, we calculated the realized heritability over the same number of selected generations, 12, for each colony. Evaluation of changes in realized heritability during selection Potential changes in the heritability of Dipel resistance among the five O. nubilalis colonies were evaluated using the method described by Tabashnik & McGaughey (1994). Data for the three Iowa colonies were divided into three periods of five to seven generations each. Data for the two Kansas colonies were divided into two periods of six generations each. Risk predictions using realized heritability estimates The number of generations, G, required to realize a 10- fold increase in LC 50 was calculated under specific selection pressures using TabashnikÕs (1992) formula: G = 1/R These calculations were based on the mean slope of probit analyses observed for the five O. nubilalis colonies when averaged across all selected generations. Resistance stability To determine if Dipel resistance would remain stable in the absence of selection pressure, a strain (KS-SC-B) derived from the KS-SC resistant strain was reared without exposure to Dipel for five generations. At initiation, the resistance was 62 at the ninth selected generation. The KS-SC-A strain (the original KS-SC strain) was maintained under intense selection with Dipel. Standard bioassays were used to monitor LC values. The mean response in the absence of selection pressure was calculated using the same approach as the mean response to selection. Results Progression of resistance selection The responses of the three Iowa colonies to selection with Dipel were similar (table 1). The resistance in the IA-1 colony reached 46 by the sixteenth selected generation and then remained at for the next four generations. The resistance in the IA-2 colony increased to 59 by the fifteenth selected generation and then remained stable for the next two selected generations. The resistance of the IA-3 colony increased to 52 by the twelfth selected generation and remained stable for the next four selected generations. The resistance of the two Kansas colonies increased somewhat faster than it occurred in the three Iowa colonies (table 1). In the KS-NE colony, the resistance reached 42 by the seventh selected generation and then remained at for the next five selected generations. In the KS-SC
3 Heritability and stability of Bt resistance in O. nubilalis 451 Table 1. Changes in susceptibility of five colonies of Ostrinia nubilalis larvae in response to Dipel incorporated in the diet a. Colony N a SP b Slope ± SE LC 50 (95% CI) RF c IA-CK d 1.6 ± ( ) IA ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) 42 IA ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) 51 IA ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) 50 KS-NE CK 1.8 ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) 35 KS-SC CK 1.9 ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) ± ( ) 66 a The selected generation number. Data for generations not shown were presented in Huang et al. (1997). Data for the sixteenth, seventeenth, and eighteenth selected generations of the IA-1 colony; the thirteenth, fourteenth, and fifteenth selected generations of the IA-2 colony; twelfth and thirteenth selected generations of the IA-3 colony; eighth and ninth selected generations of the KS-NE colony ; and the eighth, ninth, and tenth selected generations of the KS-SC colony were based on bioassays in which 128 larvae per generation were evaluated individually in 128-cell trays for each concentration. b Selection pressure recorded as percent mortality on selection diet. c Resistance factor (RF). d Unselected colony (control). colony, the resistance reached 47 by the eighth selected generation and then remained at for the next five selected generations. Analysis of realized heritability Based on all available selected generations (12 20 generations depending on the colony) the estimates of realized heritability ranged from 0.17 to 0.21 for the three Iowa and the KS-NE colonies (table 2). Based on just the first 12 selected generations, the estimates of realized heritability were for these four colonies. For the KS-SC colony, the estimate of realized heritability was 0.30, based on the first 12 selected generations. This value appeared to be somewhat higher than the realized heritabilities recorded for the other four colonies. Evaluation of change in realized heritability during selection The estimates of realized heritability for Dipel resistance in the Iowa colonies were , , and , respectively, over the three periods of selection (table 3). The estimates of realized heritability for these colonies were high during the first two periods but very low during the third period of selection. The estimates of realized heritability for the two Kansas colonies were higher during the first period of selection ( ) than during the second period ( ) (table 3). Risk predictions with realized heritability estimates The realized heritability for Dipel resistance over the period before resistance reached a plateau in each of the five O. nubilalis colonies averaged 0.29 ± Based on this level of realized heritability, resistance would increase 10-fold in nine selected generations under 70% selection mortality. The number of generations required for a 10-fold increase in LC 50 decreases as selection pressure increased (fig. 1). Determination of resistance stability In the absence of Dipel selection pressure, the resistance in the KS-SC-B strain decreased from 62 to 42 after two generations, but it remained at about that level over the next three generations (fig. 2). In the absence of selection the mean response was Discussion Dipel resistance in the five selected colonies of O. nubilalis appeared to plateau at after selected generations. Resistance to B. thuringiensis endotoxins reported for other insects ranged from 1.1 to 10,000 (Tabashnik, 1994; Bauer, 1995; Huang et al., 1999a). Thus, Dipel resistance in our O. nubilalis colonies could be ranked as a moderate level of resistance. The prior field exposure of these five O. nubilalis colonies to B. thuringiensis insecticides is unknown, but is believed to be very low. In Kansas, the use of B. thuringiensis microbial formulations by farmers on field corn was below detectable levels in the most recent pesticide use surveys (Cress, 1991, 1998). The field exposure of four of these populations to other foliar pesticides is also believed to be minimal. However, the population from south central Kansas may have been exposed to various non-bt foliar insecticide treatments (organophosphates, carbamates, and pyrethroids) on an annual basis over the past years. Note that the population with the highest exposure to pesticides is also the population that developed the highest Dipel resistance and is the population characterized by the highest realized heritability. Tabashnik (1992) calculated the realized heritability for 27 different selection experiments that involved nine different insect species. He obtained realized heritability values that
4 452 F. Huang et al. Table 2. Realized heritability, h 2, and parameters used to calculate the realized heritability of Dipel resistance in Ostrinia nubilalis a. Colony Response Selection differential N LC 50 (1) LC 50 (2) R p i Mean slope S h 2 IA IA IA KS-NE KS-SC a N is the number of selected generation included in each calculation; LC 50 (1) and LC 50 (2) are the initial and final LC 50 s; R is the mean response to selection; p is the mean percentage surviving selection; i is the intensity of selection; and S is the selection differential. Table 3. Changes in realized heritability, h 2, of Dipel resistance in Ostrinia nubilalis during selection a. Colony N 1 N 2 R S h 2 IA IA IA KS-NE KS-SC a N 1 is the initial selection and N 2 is the final selection for the selection period in question. LC 50 (1) and LC 50 (2) are the initial and final LC 50 s; R is the mean response to selection; and S is the selection differential. ranged from to 0.61 (mean = 0.19). Our estimates of realized heritability for Dipel resistance in O. nubilalis colonies ranged from 0.17 to 0.30 (mean = 0.21), which is about average among the reported realized heritabilities. The realized heritability for Dipel resistance in the three Iowa colonies was high ( ) during the first two selection periods, but was low ( ) during the third selection period. This suggests that the frequency of the allele or alleles conveying resistance in these O. nubilalis colonies was initially relatively low, but increased gradually during the first two selection periods and then it approached homozygous condition during the third selection period (Firko & Hayes, 1990). The realized heritability of Dipel resistance in the two Kansas colonies was high ( ) during the first selection period, but was low (0 0.06) during the second period (table 3). This suggests that the initial allele frequency for resistance to Dipel was higher in the Kansas colonies than it was in the Iowa colonies and that it approached the homozygous condition during the second selection period. The high realized heritability for the KS-SC colony corresponds with the colony with the most rapid development of resistance and the highest level of resistance among the five tested colonies. The realized heritability did not appear to be associated with selection pressure. For the Iowa colonies the selection pressure averaged 94 ± 1% (mean ± SD) mortality during the third selection period, which was higher than the selection pressure during the first and second selection periods which averaged 82 ± 8% mortality. The mean response, R, (0.03 ± 0.02) was considerably lower during the third period than during the first and second periods (0.12 ± 0.04). These results suggest that it will be important to compare realized heritabilities during the period when resistance is changing most rapidly. The estimates of realized heritability for Dipel resistance in O. nubilalis decreased as the number of selected generations increased, since resistance appeared to reach a plateau during the selection experiments. This was especially true for the Kansas colonies. Stability of resistance to B. thuringiensis endotoxins has been examined in several other insects. In most cases, resistance declines when the selection pressure is removed, but the decline is incomplete and seldom returns to preselection levels (McGaughey & Beeman, 1988; Tabashnik et al., 1991; Tabashnik, 1994; Rahardja & Whalon, 1995; Müller-Cohn et al., 1996; Tang et al., 1997). Dipel resistance in the KS-SC-B strain remained relatively stable over five generations. The mean response in the absence of selection during the stability experiment was a small negative value ( 0.031) compared to the response during selection for resistance (0.15) (table 2). The most likely cause of instability of resistance to B. thuringiensis endotoxins suggested for other insects is the presence of fitness costs which are commonly associated with resistance to B. thuringiensis endotoxins (Tabashnik, 1994). It is possible that selection was relaxed before the gene for resistance became homozygous or fixed for resistance. This would allow selection to favour the gene for non-resistance in the absence of selection pressure. Laboratory selection experiments may not necessarily reflect the rates or mechanisms likely to occur in resistance development under field conditions. However, laboratory selection is a valuable tool for the assessment of potential risk of resistance development (Bauer, 1995). Our results are also interesting because some of the endotoxins derived from B. thuringiensis have been engineered for expression in several crop plants including corn (Ostlie et al., 1997). Most transgenic Bt corn hybrids have been engineered to express
5 Heritability and stability of Bt resistance in O. nubilalis 453 Fig. 1. The number of generations of Ostrinia nubilalis required to produce a 10-fold increase in LC 50 at a realized heritability of 0.3 and exposed to selection pressures of 30 99% mortality with Dipel ES. the Cry1Ab endotoxin of B. thuringiensis. The efficacy of some Bt-corn hybrids against O. nubilalis is remarkable (Ostlie et al., 1997) and widespread adoption of the technology is occurring. Many researchers believe that the use of transgenic Bt-plants will increase selection for resistance in pests such as O. nubilalis, because selection pressure is much higher on transgenic plants than on plants treated with B. thuringiensis microbial insecticides (McGaughey & Whalon, 1992; Tabashnik, 1994; Bauer, 1995; Gould, 1998). Based on the available evidence, there appears to be a high potential for resistance development to B. thuringiensis in O. nubilalis. First, there was a rapid decrease in susceptibility to Dipel in all five tested colonies of O. nubilalis (Huang et al., 1997). Second, there was a period of relative stability in the resistance in the absence of continued selection pressure. Third, the resistance appeared to be inherited as a partially dominant trait (Huang et al., 1999b). Fourth, the resistance had moderate levels of heritability. Fifth, the colony from the region with the highest pesticide exposure developed the highest Dipel resistance and the highest heritability for this resistance. Therefore, it would seem prudent to develop and implement a scientifically sound resistance management strategy for use with transgenic crops that utilize B. thuringiensis endotoxins. We need to avoid or at least delay the development of resistance to B. thuringiensis endotoxins in O. nubilalis. Resistance management will need to be deployed early in the commercialisation of transgenic crops to maintain the effectiveness of this very promising management tool. The results reported here must be interpreted with caution in relation to their application to O. nubilalis resistance to Bt corn. These laboratory selected Dipelresistant corn borer will need to be tested for their ability to survive on different Bt corn lines. Acknowledgements We thank Dr William H. McGaughey (USDA-ARS), Dr Theodore L. Hopkins and Dr James Schwenke (statistics) for Fig. 2. Stability of Dipel resistance (resistance factors) of the KS- SC colony of Ostrinia nubilalis after removal of selection pressure. A: KS-SC-A strain (also called KS-SC) selected using Dipel ES. B: KS-SC-B strain, derived from the resistant KS-SC strain after nine selected generations, and then reared for five generations without Dipel ES selection pressure. helpful suggestions during this study. The authors also are grateful to Dr William H. McGaughey, Dr Gerald Wilde, Dr Srini Kambhampati and two anonymous reviewers for constructive comments on this article. Appreciation is also extended to the USDA Corn Insects Laboratory in Ames, Iowa, for providing some of the O. nubilalis egg masses needed to establish the Iowa colonies. This article is Contribution No J from the Kansas Agricultural Experiment Station and represents work sponsored by F- 205; NC-205; and the Kansas Corn Commission (Contract No. 1294, Kansas Department of Agriculture). Voucher specimens, Voucher No. 079, are located in the Kansas State University Museum of Entomological and Prairie Arthropod Research. References Bauer, L.S. (1995) Resistance: a threat to the insecticidal crystal proteins of Bacillus thuringiensis. Florida Entomologist 78, Cress, D.C. (1991) 1990 corn and soybean summary. Kansas agricultural chemical usage. Cooperative Extensive Service, Kansas State University, Manhattan, Kansas, USA. Cress, D.C. (1998) 1996 corn pesticide summary. Kansas agricultural chemical usage. Cooperative Extensive Service, Kansas State University, Manhattan, Kansas, USA. Falconer, D.S. (1981) Introduction to quantitative genetics. 2nd edn. New York, Longman. Firko, M.J. & Hayes, J.L. (1990) Quantitative genetic tools for insecticide resistance risk assessment: estimating the heritability of resistance. Journal of Economic Entomology 83, Gould, F. (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annual Review of Entomology 43, Guthrie, W.D., Raun, E.S., Dicke, F.F., Pesho, G.R. & Carter, S.W. (1965) Laboratory production of European corn borer egg masses. Iowa State Journal of Science 40,
6 454 F. Huang et al. Huang, F., Higgins, R.A. & Buschman, L.L. (1997) Baseline susceptibility and changes in susceptibility to Bacillus thuringiensis subsp. kurstaki under selection pressure in European corn borer (Lepidoptera: Pyralidae). Journal of Economic Entomology 90, Huang, F., Higgins, R.A. & Buschman, L.L. (1999a) Transgenic Bt-plants: successes, challenges and strategies. Proceedings, The Second Asia Pacific Crop Protection Conference, Pestology 23, Huang, F., Buschman, L.L., Higgins, R.A., & McGaughey, W.H. (1999b) Inheritance of resistance to Bacillus thuringiensis toxin (Dipel ES) in the European corn borer. Science 284, McGaughey, W.H. & Beeman, R.W. (1988) Resistance to Bacillus thuringiensis in colonies of Indianmeal moth and almond moth (Lepidoptera: Pyralidae). Journal of Economic Entomology 81, McGaughey, W.H. & Whalon, M.E. (1992) Managing insect resistance to Bacillus thuringiensis toxins. Science 258, Müller-Cohn, J., Chaufaux, J., Buisson, C., Gilois, N., Sanchis, V. & Lerechus, D. (1996) Spodoptera littoralis Boisduval (Lepidoptera: Noctuidae) resistance to CryIC and crossresistance to other Bacillus thuringiensis crystal toxins. Journal of Economic Entomology 89, Omer, A.D., Tabashnik, B.E., Johnson, M.W. & Leigh, T.F. (1993) Realized heritability of resistance to dicrotophos in greenhouse whitefly. Entomologia Experimentalis et Applicata 68, Ostlie, K.R., Hein, G.L., Higley, L.G., Kaster, L.V. & Showers, W.B. (1984) European corn borer (Lepidoptera: Pyralidae) development, larval survival, and adult vigor on meridic diets containing marker dyes. Journal of Economic Entomology 77, Ostlie, K.R., Hutchison, W.D. & Hellmich, R.L. (Eds) (1997) Btcorn and European corn borer. Long term success through resistance management. North Central Region Extension Publication NCR 602. Rahardja, U. & Whalon, M.E. (1995) Inheritance of resistance to Bacillus thuringiensis subsp. tenebrionis -endotoxin in the Colorado potato beetle (Coleoptera: Chrysomelidae) Journal of Economic Entomology 88, Reed, G.L., Showers, W.B., Huggans, J.L. & Carter, S.W. (1972) Improved procedures for mass rearing the European corn borer. Journal of Economic Entomology 65, SAS Institute (1990) SAS/STAT user s guide. Version 6, 4th edn. SAS Institute, Cary, North Carolina. Tabashnik, B.E. (1992) Resistance risk management: realized heritability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae), tobacco budworm (Lepidoptera: Noctuidae), and Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology 85, Tabashnik, B.E. (1994) Evolution of resistance to Bacillus thuringiensis. Annual Review of Entomology 39, Tabashnik, B.E. & McGaughey, W.H. (1994) Resistance risk assessment for single and multiple insecticides: responses of Indianmeal moth (Lepidoptera: Pyralidae) to Bacillus thuringiensis. Journal of Economic Entomology 87, Tabashnik, B.E., Finson, N. & Johnson, M.W. (1991) Managing resistance to Bacillus thuringiensis: lessons from the diamondback moth (Lepidoptera: Plutellidae). Journal of Economic Entomology 84, Tanaka, Y. & Noppun, V. (1989) Heritability estimates of phenthoate resistance in the diamondback moth. Entomologia Experimentalis et Applicata 52, Tang, J.D., Gilboa, S., Roush, R.T. & Shelton, A.S. (1997) Inheritance, stability, and lack-of-fitness costs of fieldselected resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae) from Florida. Journal of Economic Entomology 90, (Accepted 30 May 1999) CAB International, 1999
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