Skip to main content
SpringerLink
Log in

Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis

  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Farmers, industry, governments and environmental groups agree that it would be useful to manage transgenic crops producing insecticidal proteins to delay the evolution of resistance in target pests. The main strategy proposed for delaying resistance to Bacillus thuringiensis (Bt) toxins in transgenic crops is the high-dose/refuge strategy. This strategy is based on the unverified assumption that resistance alleles are initially rare (<10–3). We used an F2 screen on >1,200 isofemale lines of Ostrinia nubilalis Hübner (Lepidoptera: Crambidae) collected in France and the US corn belt during 1999–2001. In none of the isofemale lines did we detect alleles conferring resistance to Bt maize producing the Cry1Ab toxin. A Bayesian analysis of the data indicates that the frequency of resistance alleles in France was <9.20 × 10–4 with 95% probability, and a detection probability of >80%. In the northern US corn belt, the frequency of resistance to Bt maize was <4.23 × 10–4 with 95% probability, and a detection probability of >90%. Only 95 lines have been screened from the southern US corn belt, so these data are still inconclusive. These results suggest that resistance is probably rare enough in France and the northern US corn belt for the high-dose plus refuge strategy to delay resistance to Bt maize.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1A–E.

Similar content being viewed by others

References

  • Alstad DN, Andow DA (1995) Managing the evolution of insect resistance to transgenic plants. Science 268:1894–1896

    CAS  Google Scholar 

  • Andreev D, Kreitman M, Phillips TW, Beeman RW, ffrench-Constant RH (1999) Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). J Mol Evol 48:615–624

    CAS  PubMed  Google Scholar 

  • Andow DA (2001) Resisting resistance to Bt corn. In: Letourneau DK, Burrows BE (eds) Genetically engineered organisms: assessing environmental and human health effects. CRC Press, Boca Raton, Florida, pp 99–124

    Google Scholar 

  • Andow DA, Alstad DN (1998) F2 screen for rare resistance alleles. J Econ Entomol 9:572–578

    Google Scholar 

  • Andow DA, Alstad DN (1999) Credibility interval for rare resistance allele frequencies. J Econ Entomol 92:755–758

    Google Scholar 

  • Andow DA, Alstad DN, Pang Y-H, Bolin PC, Hutchinson WD (1998) Using an F2 screen to search for resistance alleles to Bacillus thuringiensis toxin in European corn borer (Lepidoptera: Crambidae). J Econ Entomol 91:579–584

    Google Scholar 

  • Andow DA, Olson DM, Hellmich II RL, Alstad DN, Hutchinson WD (2000) Frequency of resistance alleles to Bacillus thuringiensis toxin in an Iowa population of European corn borer. J Econ Entomol 93:26–30

    CAS  Google Scholar 

  • Bolin PC (1998) Durability of Bacillus thuringiensis transgenic corn for management of the European corn borer (Lepidoptera: Crambidae). PhD thesis, University of Minnesota, St. Paul, Minnesota

  • Bourguet D, Génissel A, Raymond M (2000a) Insecticide resistance and dominance levels. J Econ Entomol 93:1588–1595

    CAS  PubMed  Google Scholar 

  • Bourguet D, Bethenod M-T, Pasteur N, Viard F (2000b) Gene flow in the European corn borer Ostrinia nubilalis: implications for the sustainability of transgenic insecticidal maize. Proc R Soc Lond B 267:117–122

    Article  CAS  PubMed  Google Scholar 

  • Bentur JS, Andow DA, Cohen MB, Romena AM, Gould F (2000) Frequency of alleles conferring resistance to a Bacillus thuringiensis toxin in a Philippines population of Scirpophaga incertulas (Lepidoptera: Pyralidae). J Econ Entomol 93:1515–1521

    CAS  PubMed  Google Scholar 

  • Caprio MA (1998) Evaluating resistance management strategies for multiple toxins in the presence of external refuges. J Econ Entomol 91:1021–1031

    Google Scholar 

  • Comins HN (1977) The management of pesticide resistance. J Theor Biol 65:399–420

    CAS  PubMed  Google Scholar 

  • Coustau C, Chevillon C, ffrench-constant RH (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends Ecol Evol 15:378–383

    Article  PubMed  Google Scholar 

  • Crow JF, Kimura M (1970) An introduction to population genetics theory. Harper and Row, New York

  • Environmental Protection Agency (EPA) (1998) The Environmental Agency's White Paper on Bt Plant-Resistance Management, 14 January 1998. US EPA, Washington, District of Columbia

  • ffrench-Constant RH (1994) The molecular and population genetics of cyclodiene resistance. Insect Biochem Mol Biol 24:335–345

    CAS  PubMed  Google Scholar 

  • Gahukar RT (1975) Nouvelles techniques adoptées pour l'élevage d'Ostrinia nubilalis Hübner sur milieu artificiel. Ann Zool Ecol Anim 7:491–498

    Google Scholar 

  • Georghiou GP, Lagunes-Tejeda A (1991) The occurrence of resistance to pesticides in arthropods. Food and Agriculture Organization, Rome

  • Gould F (1998) Sustainability of transgenic insecticidal cultivars: integrating pest genetics and ecology. Annu Rev Entomol 43:701–726

    CAS  Google Scholar 

  • Gould F, Anderson A, Jones A, Sumerford D, Heckel DG, Lopez J, Micinski S, Leonard R, Laster M (1997) Initial frequency of alleles for resistance to Bacillus thuringiensis toxins in field populations of Heliothis virescens. Proc Natl Acad Sci USA 94:3519–3523

    Article  CAS  PubMed  Google Scholar 

  • Guillemaud T, Rooker S, Pasteur N, Raymond M (1996) Testing the unique amplification event and the worldwide migration hypothesis of insecticide resistance genes with sequence data. Heredity 77:535–543

    CAS  PubMed  Google Scholar 

  • Guthrie WD, Dicke FF, Neiswander CR (1960) Leaf sheath feeding resistance to the European corn borer in eight inbred lines of dent corn. Ohio Agric Exp Stn Res Bull 860

  • Hurley TM, Babcock BA, Hellmich II RL (1997) Biotechnology and pest resistance: an economic assessment of refuges. 97-W, Center for Agricultural and Rural Development, Ames, Iowa

  • James C (2000) Global status of commercialized transgenic crops: 2000. ISAAA Briefs No. 21: Preview. ISAAA, Ithaca, New York

  • Krattiger AF (1997) Insect resistance in crops: a case study of Bacillus thuringiensis (Bt) and its transfer to developing countries. ISAAA Briefs No. 2. ISAAA, Ithaca, New York

  • Leahy TC, Andow DA (1994) Egg weight, frcundity, and longevity are increased by adult feeding in Ostrinia nubilalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am 87:342–349

    Google Scholar 

  • Lereclus D, Arantes O, Chaufaux J, Lecadet MM (1989) Transformation and expression of a cloned delta-endotoxin gene in Bacillus thuringiensis. FEMS Microbiol Lett 60:211–218

    CAS  Google Scholar 

  • McKenzie JA (1996) Ecological and evolutionary aspects of insecticide resistance. R.G. Landes, Georgetown, Texas

  • Mallet J, Porter P (1992) Preventing insect adaptation to insect-resistant crops: are seed mixtures or refugia the best strategy? Proc Roy Soc Lond B 250:165–169

    Google Scholar 

  • National Agricultural Statistical Service (NASS) (2000) Prospective plantings, March 31, 2000. NASS, Agricultural Statistics Board, USDA, Washington, District of Columbia

  • Onstad DW, Gould F (1998) Modelling the dynamics of adaptation to transgenic maize by European corn borer (Lepidoptera: Pyralidae). J Econ Entomol 91:585–593

    Google Scholar 

  • Onstad DW, Guse CA (1999) Economic analysis of transgenic maize and nontransgenic refuges for managing European corn borer (Lepidoptera: Pyralidae). J Econ Entomol 92:1256–1265

    Google Scholar 

  • Orr HA, Betancourt AJ (2001) Haldane's sieve and adaptation from the standing genetic variation. Genetics 157:875–884

    CAS  PubMed  Google Scholar 

  • Peck SL, Gould F, Ellner SP (1999) Spread of resistance in spatially extended regions of transgenic cotton: implications for management of Heliothis virescens. J Econ Entomol 92:1–16

    Google Scholar 

  • Poitout S, Buès R (1970) Elevage de plusieurs espèces de Lépidoptères Noctuidae sur milieu artificiel riche et sur milieu artificiel simplifié. Ann Zool Ecol Anim 2:79–91

    Google Scholar 

  • Raymond M, Callaghan A, Fort P, Pasteur N (1991) Worldwide migration of amplified insecticide resistance genes in mosquitoes. Nature 350:151–153

    CAS  PubMed  Google Scholar 

  • Roush RT (1994) Managing pests and their resistance to Bacillus thuringiensis: can transgenic crops be better than sprays? Biocontrol Sci Tech 4:501–516

    Google Scholar 

  • Roush RT (1998) Two-toxin strategies for management of insecticidal transgenic crops: can pyramiding succeed where pesticide mixtures have not? Phil Trans R Soc Lond B 353:1777–1786

    CAS  Google Scholar 

  • Roush RT, McKenzie JA (1987) Ecological genetics of insecticide and acaracide resistance. Annu Rev Entomol 32:361–380

    Article  CAS  PubMed  Google Scholar 

  • Sanchis V, Lereclus D, Menou G, Chaufaux J, Lecadet MM (1988) Multiplicity of delta-endotoxin genes with different insecticidal specificities in Bacillus thuringiensis. Mol Microbiol 2:393–404

    CAS  PubMed  Google Scholar 

  • Scientific Committee on Plants (SCP) (1999) Opinion of the SCP on Bt – Resistance monitoring opinion expressed on 4 March 1999

  • Schneider JC (1999) Confidence interval for Bayesian estimates of resistance allele frequencies. J Econ Entomol 92:755

    Google Scholar 

  • Siegfried BD, Marçon PCRG, Witkowski JF, Wright RJ, Warren GW (1995) Susceptibility of field populations of the European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae), to Bacillus thuringiensis (Berliner). J Agric Entomol 12:267–273

    Google Scholar 

  • Steffey KL, Rice ME, All J, Andow DA, Gray ME, Van Duyn JW (eds) (1999) Handbook of corn insects. Entomological Society of America, Lanham, Maryland

  • Tabashnik BE, Croft BA (1982) Managing pesticide resistance in crop-arthropod complexes: interactions between biological and operational factors. Environ Entomol 11:1137–1144

    Google Scholar 

  • Tabashnik BE, Liu Y-B, Finson N, Masson L, Heckel DG (1997) One gene in diamondback moth confers resistance to four Bacillus thuringiensis toxins. Proc Natl Acad Sci USA 94:1640–1644

    Article  CAS  PubMed  Google Scholar 

  • Tabashnik BE, Patin AL, Dennehy TJ, Liu Y-B, Carrière Y, Sims MA, Antilla L (2000) Frequency of resistance to Bacillus thuringiensis in field populations of pink bollworm. Proc Natl Acad Sci USA 97:12,980–12,984

    Article  PubMed  Google Scholar 

  • Wolfenbarger LL, Phifer PR (2000) Biotechnology and ecology – The ecological risks and benefits of genetically engineered plants. Science 290:2088–2093

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations, volume 2. The theory of gene frequencies. University Chicago Press, Chicago

Download references

Acknowledgements.

We thank M. Gohar, F. Gould, D. Heckel, D. Lereclus, C. Nielsen-LeRoux, B. Tabashnik and one anonymous reviewer for comments on this manuscript. We also thank Marie-Thérèse Bethenod, Magali Calabre, Marc Delos and Gaël Magnanon for helping in sampling and in carrying out the screens in France, and Justin Duris, Mark Galatowicz, Faith Hassinger, Beth Peterson, Jacob Roark, Scott Smith and Eleanore Wesserte for helping in sampling and carrying out the Minnesota screens. We finally thank Vincent Sanchis for providing the B. thuringiensis strain, Michael Catangui for helping us locate a sampling site in South Dakota and Bruce Potter and Lee French for helping with the blacklight traps at Lamberton, Minnesota. This work was supported by the INRA AIP "Organismes Génétiquement Modifés et Environnement" and by the MENRT A.O. "Impact des OGM" to D.B., and USDA-NRI Grant 99-35302-7937 to D.A.A. and W. D. Hutchison.

Author information

Authors and Affiliations

  1. Unité de Recherches de Lutte biologique, INRA La Minière, 78 285 Guyancourt, France

    D. Bourguet, J. Chaufaux, M. Séguin & C. Buisson

  2. Department of Entomology, University of Minnesota, St. Paul, MN 55108, USA

    J. L. Hinton, T. J. Stodola & D. A. Andow

  3. Minnesota Center for Community Genetics, University of Minnesota, USA

    T. J. Stodola

  4. Department of Entomology, Texas A & M University, College Station, TX, USA

    P. Porter & G. Cronholm

  5. Department of Entomology, Kansas State University, Garden City, KS 62846, USA

    L. L. Buschman

Authors
  1. D. Bourguet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Chaufaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Séguin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Buisson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. L. Hinton
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. J. Stodola
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. P. Porter
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. Cronholm
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. L. L. Buschman
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. D. A. Andow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to D. Bourguet.

Additional information

Communicated by D. Hoisington

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bourguet, D., Chaufaux, J., Séguin, M. et al. Frequency of alleles conferring resistance to Bt maize in French and US corn belt populations of the European corn borer, Ostrinia nubilalis. Theor Appl Genet 106, 1225–1233 (2003). https://doi.org/10.1007/s00122-002-1172-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-002-1172-1

Keywords

Search

Navigation