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Contamination and management of resistance evolution to high-dose transgenic insecticidal crops

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Abstract

For maize and cotton, transgenic varieties that express toxins derived from Bacillus thuriengensis (Bt) are now planted in several countries. To slow resistance evolution, the “high-dose/refuge” strategy is broadly implemented in which resistance is recessive and some fields (or areas within fields) are planted exclusively with Bt crops and other fields planted exclusively with non-transgenic refuge crops for susceptible insects. This strategy, however, could potentially be undermined by contamination. Here, we investigate general models of resistance evolution for high-dose events in which fields are contaminated due to the inadvertent mixing of seeds, volunteer plants, or pollen flow between Bt and non-Bt varieties coupled with seed-saving by farmers. Contamination of the refuge by Bt plants increases selection for resistance, thereby speeding resistance evolution. Nonetheless, in most situations this effect is small. Contamination of Bt fields by non-transgenic plants might be expected to have the opposite effect and always reduce the rate of resistance evolution. While this is often the case, it is not always so. If larvae move among plants within a field, then high movement rates may reverse the effect of contamination of Bt fields to slow resistance evolution. Furthermore, if the dispersal rates of adult females between Bt and refuge fields are low, then contamination of Bt fields may speed resistance. These results suggest that contamination has the potential to undermine the efficacy of the high-dose/refuge strategy, yet depending upon the particular pest and situation, contamination may not be a concern.

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References

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

    Article  PubMed  CAS  Google Scholar 

  • Bagla P (2010) Hardy cotton-munching pests are latest blow to GM crops. Science 327:1439

    Article  PubMed  CAS  Google Scholar 

  • Barbosa P, Krischik V, Lance D (1989) Life-history traits of forest-inhabiting flightless lepidoptera. Am Midl Nat 122:262–274

    Article  Google Scholar 

  • Berger A (1992) Larval movements of Chilo partellus (Lepidoptera: Pyralidae) within and between plants—timing, density responses and survival. Bull Entomol Res 82:441–448

    Article  Google Scholar 

  • Caprio MA (2001) Source-sink dynamics between transgenic and non-transgenic habitats and their role in the evolution of resistance. J Econ Entomol 94:698–705

    Article  PubMed  CAS  Google Scholar 

  • Caprio MA, Sumerford DV, Simms SR (2000) Evaluating transgenic plants for suitability in pest and resistance management programs. In: Lacey L, Kaya H (eds) Field manual of techniques in invertebrate pathology. Kluwer, Boston, pp 805–828

    Google Scholar 

  • Carrière Y, Ellers-Kirk C, Sisterson M, Antilla L, Whitlow M, Dennehy TJ, Tabashnik BE (2003) Long-term regional suppression of pink bollworm by Bacillus thuringiensis cotton. Proc Natl Acad Sci U S A 100:1519–1523

    Article  PubMed  Google Scholar 

  • Carrière YP, Dutilleul P, Ellers-Kirk C, Pedersen B, Haller S, Antilla L, Dennehy TJ, Tabashnik BE (2004) Sources, sinks, and the zone of influence of refuges for managing insect resistance to Bt crops. Ecol Appl 14:1615–1623

    Article  Google Scholar 

  • Chilcutt CF, Tabashnik BE (2004) Contamination of refuges by Bacillus thuringiensis toxin genes from transgenic maize. Proc Natl Acad Sci U S A 101:7526–7529

    Article  PubMed  CAS  Google Scholar 

  • Cohen MB, Romena AM, Gould F (2000) Dispersal by larvae of the stem borers Scirpophaga incertulas (Lepidoptera: Pyralidae) and Chilo suppressalis (Lepidoptera: Crambidae) in plots of transplanted rice. Environ Entomol 29:958–971

    Article  Google Scholar 

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

    Google Scholar 

  • Davis PM, Onstad DW (2000) Seed mixtures as a resistance management strategy for European corn borer (Lepidoptera: Crambidae) infesting transgenic corn expressing cry1Ab protein. J Econ Entomol 93:937–948

    Article  PubMed  CAS  Google Scholar 

  • Dirie AM, Cohen MB, Gould F (2000) Larval dispersal and survival of Scirpophaga incertulas (Lepidoptera: Pyralidae) and Chilo suppressalis (Lepidoptera: Crambidae) on cry1Ab-transformed and non-transgenic rice. Environ Entomol 29:972–978

    Article  Google Scholar 

  • Downes S, Mahon RJ, Rossiter L, Kauter G, Leven T, Fitt G, Baker G (2010a) Adaptive management of pest resistance by Helicoverpa species (Noctuidae) in Australia to the Cry2Ab Bt toxin in Bollgard II (R) cotton. Evol Appl 3:574–584

    Article  Google Scholar 

  • Downes S, Parker T, Mahon R (2010b) Incipient resistance of Helicoverpa punctigera to the Cry2Ab Bt toxin in Bollgard II (R) cotton. PloS One 5:e12567

    Article  PubMed  Google Scholar 

  • Ellstrand NC (2003) Dangerous liaisons? When cultivated plants mate with their wild relatives. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Ellstrand NC, Hoffman CA (1990) Hybridization as an avenue of escape for engineered genes—strategies for risk reduction. Bioscience 40:438–442

    Article  Google Scholar 

  • Ellstrand NC, Prentice HC, Hancock JF (1999) Gene flow and introgression from domesticated plants into their wild relatives. Annu Rev Ecol Syst 30:539–563

    Article  Google Scholar 

  • Fadamiro HY, Baker TC (1999) Reproductive performance and longevity of female European corn borer, Ostrinia nubilalis: effects of multiple mating, delay in mating, and adult feeding. J Insect Physiol 45:385–392

    Article  PubMed  CAS  Google Scholar 

  • Fitt GP, Andow DA, Carrière Y, Moar WJ, Schuler TH, Omoto C, Kanya J, Okech MA, Arama P, Maniania NK (2004) Resistance risks and management associated with Bt maize in Kenya. In: Hilbeck A, Andow DA (eds) Environmental risk assessment of transgenic organisms: a case study of Bt Maize in Kenya. CABI, Wallingford, pp 209–250

    Google Scholar 

  • Friesen LF, Nelson AG, Van Acker RC (2003) Evidence of contamination of pedigreed canola (Brassica napus) seedlots in western Canada with genetically engineered herbicide resistance traits. Agron J 95:1342–1347

    Article  Google Scholar 

  • Gassman AJ, Carrière Y, Tabashnik BE (2009) Fitness costs of insect resistance to Bacillus thuringiensis. Annu Rev Entomol 54:127–145

    Article  Google Scholar 

  • Georghiou GP, Taylor CE (1986) Factors influencing the evolution of resistance. In: Council NR (ed) Pesticide resistance: strategies and tactics for management. National Academy Press, Washington, D.C., pp 157–169

    Google Scholar 

  • Gould F, Martinezramirez A, Anderson A, Ferre J, Silva FJ, Moar WJ (1992) Broad-spectrum resistance to Bacillus thuringiensis toxins in Heliothis virescens. Proc Natl Acad Sci U S A 89:7986–7990

    Article  PubMed  CAS  Google Scholar 

  • Gould F, Anderson A, Reynolds A, Bumgarner L, Moar W (1995) Selection and genetic analysis of a Heliothis virescens (Lepidoptera, Noctuidae) strain with high levels of resistance to Bacillus thuringiensis toxins. J Econ Entomol 88:1545–1559

    CAS  Google Scholar 

  • Hassell MP (1975) Density dependence in single-species populations. J Anim Ecol 44:283–295

    Article  Google Scholar 

  • Haygood R, Ives AR, Andow AD (2003) Consequences of recurrent gene flow from crops to wild relatives. Proc R Soc Lond B 270:1879–1886

    Article  Google Scholar 

  • Heuberger S, Ellers-Kirk C, Yafuso C, Gassmann AJ, Tabashnik BE, Dennehy TJ, Carrière Y (2008) Effects of refuge contamination by transgenes on Bt resistance in pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 101:504–514

    Article  PubMed  Google Scholar 

  • Hibbard BE, Duran DP, Ellersieck MR, Ellsbury MM (2003) Post-establishment movement of western corn rootworm larvae (Coleoptera: Chrysomelidae) in Central Missouri corn. J Econ Entomol 96:599–608

    Article  PubMed  Google Scholar 

  • Hibbard BE, Higdon ML, Duran DP, Schweikert YM, Ellersieck MR (2004) Role of egg density on establishment and plant-to-plant movement by western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 97:871–882

    Article  PubMed  CAS  Google Scholar 

  • Hibbard BE, Vaughn TT, Oyediran IO, Clark TL, Ellersieck MR (2005) Effect of Cry3Bbl-expressing transgenic corn on plant-to-plant movement by western corn rootworm larvae (Coleoptera: Chrysomelidae). J Econ Entomol 98:1126–1138

    Article  PubMed  CAS  Google Scholar 

  • Hinton HE (1981) Biology of insect eggs, volumes I, II, III. Pergamon, Oxford

    Google Scholar 

  • Hu Y (2008) Dispersal and mating system of European corn borer, Ostrinia nubilalis (Hübner) [Lepidoptera: Crambidae], in relation to Bt resistance management. University of Minnesota, Twin Cities

    Google Scholar 

  • Huang FN, Leonard BR, Andow DA (2007) Sugarcane borer (Lepidoptera: Crambidae) resistance to transgenic Bacillus thuringiensis maize. J Econ Entomol 100:164–171

    Article  PubMed  Google Scholar 

  • Hunt TE, Higley LG, Witkowski JF, Young LJ, Hellmich RL (2001) Dispersal of adult European corn borer (Lepidoptera: Crambidae) within and proximal to irrigated and non-irrigated corn. J Econ Entomol 94:1369–1377

    Article  Google Scholar 

  • Hurley TM, Babcock BA, Hellmich RL (2001) Bt corn and insect resistance: an economic assessment of refuges. J Agric Resour Econ 26:176–194

    Google Scholar 

  • Hutchison WD, Burkness EC, Mitchell PD, Moon RD, Leslie TW, Fleischer SJ, Abrahamson M, Hamilton KL, Steffey KL, Gray ME, Hellmich RL, Kaster LV, Hunt TE, Wright RJ, Pecinovsky K, Rabaey TL, Flood BR, Raun ES (2010) Areawide suppression of European corn borer with Bt maize reaps savings to non-Bt maize growers. Science 330:222–225

    Article  PubMed  CAS  Google Scholar 

  • IPGRI (2004) Final report on technical issues associated with the development of CGIAR policies to address the possibility of adventitious presence of transgenes in CGIAR ex situ collections. International Plant Genetic Resources Institute, Rome

    Google Scholar 

  • Ives AR, Andow DA (2002) Evolution of resistance to Bt crops: directional selection in structured environments. Ecol Lett 5:792–801

    Article  Google Scholar 

  • Ives AR, Glaum PR, Ziebarth NL, Andow DA (2011) The evolution of resistance to two-toxin pyramid transgenic crops. Ecol Appl (in press)

  • James C, Brief 41: Global Status of Commercialized Biotech/GM Crops (2009) International service for the acquisition of agri-biotech applications, 2009

  • Kim KS, Bagley MJ, Coates BS, Hellmich RL, Sappington TW (2009) Spatial and temporal genetic analyses show high gene flow among European corn borer (Lepidoptera: Crambidae) populations across the central US corn belt. Environ Entomol 38:1312–1323

    Article  PubMed  CAS  Google Scholar 

  • Kruger M, Van Rensburg JBJ, Van den Berg J (2009) Perspective on the development of stem borer resistance to Bt maize and refuge compliance at the Vaalharts irrigation scheme in South Africa. Crop Prot 28:684–689

    Article  Google Scholar 

  • Lamkey K (2004) Seed production in corn and soybean. In: Andow DA (ed) A growing concern: protecting the food supply in an era of pharmaceutical and industrial crops. Union of Concerned Scientists, Boston, pp 54–74

    Google Scholar 

  • Liu YB, Tabashnik BE, Dennehy TJ, Patin AL, Sims MA, Meyer SK, Carriere Y (2001) Effects of Bt cotton and Cry1Ac toxin on survival and development of pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 94:1237–1242

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mellon M, Rissler J (2004) Gone to seed: transgenic contaminants in the traditional seed supply. Union of Concerned Scientists, Cambridge

    Google Scholar 

  • Muhammed L, Underwood E (2004) The maize agricultural context in Kenya. In: Hilbeck A, Andow DA (eds) Environmental risk assessment of transgenic organisms: a case study of Bt Maize in Kenya. CABI, Wallingford, pp 21–56

    Google Scholar 

  • Nieswander CR, Huber LL (1929) Height and silking as factors influencing European corn borer population. Ann Entomol Soc Am 22:527–542

    Google Scholar 

  • Onstad DW (2006) Modeling larval survival and movement to evaluate seed mixtures of transgenic corn for control of western corn rootworm (Coleoptera: Chrysomelidae). J Econ Entomol 99:1407–1414

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Parker CD, Luttrell RG (1999) Interplant movement of Heliothis virescens (Lepidoptera: Noctuidae) larvae in pure and mixed plantings of cotton with and without expression of the Cry1Ac delta-endotoxin protein of Bacillus thuringiensis Berliner. J Econ Entomol 92:837–845

    PubMed  Google Scholar 

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

    Google Scholar 

  • Ross SE, Ostlie KR (1990) Dispersal and survival of early instars of European corn borer (Lepidoptera: Pyralidae) in field corn. J Econ Entomol 83:831–836

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sisterson MS (2005) Evolution of resistance to transgenic crops: interactions between insect movement and field distribution. J Econ Entomol 98:1751–1762

    Article  PubMed  Google Scholar 

  • Tabashnik BE (1994a) Delaying insect adaptation to transgenic plants—seed mixtures and refugia reconsidered. Proc R Soc Lond B Biol Sci 255:7–12

    Article  Google Scholar 

  • Tabashnik BE (1994b) Evolution of resistance to Bacillus thuringiensis. Annu Rev Entomol 39:47–79

    Article  Google Scholar 

  • Tabashnik BE, Carrière Y (2007) Evolution of insect resistance to transgenic plants. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, Berkeley, pp 267–279

    Google Scholar 

  • 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, Gassmann AJ, Crowder DW, Carrière Y (2008) Insect resistance to Bt crops: evidence versus theory. Nat Biotechnol 26:199–202

    Article  PubMed  CAS  Google Scholar 

  • United States Environmental Protection Agency (2001) Biopesticides registration action document: Bacillus thuringiensis (Bt) plant incorporated protectants. In: Office of Pesticide Programs B, and Pollution Prevention Division, (ed). Environmental Protection Agency

  • Vermij P (2006) Liberty link rice raises specter of tightened regulations. Nat Biotechnol 24:1301–1302

    Article  PubMed  CAS  Google Scholar 

  • Wu HH, Wu KM, Wang DY, Guo YY (2006) Flight potential of pink bollworm, Pectinophora gossypiella Saunders (Lepidoptera: Gelechiidae). Environ Entomol 35:887–893

    Article  Google Scholar 

  • Wu KM, Lu YH, Feng HQ, Jiang YY, Zhao JZ (2008) Suppression of cotton bollworm in multiple crops in china in areas with Bt toxin-containing cotton. Science 321:1676–1678

    Article  PubMed  CAS  Google Scholar 

  • Xu Z, Liu F, Chen J, Huang F, Andow DA, Shen J, Zhu YC (2009) Using an F2 screen to monitor resistance allele frequency to Bt cotton in field populations of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). Pest Manage Sci 65:391–397

    Article  CAS  Google Scholar 

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Acknowledgments

P. R. Glaum was funded in part by a United States-National Science Foundation Interdisciplinary Training for Undergraduates in Biological and Mathematical Sciences grant to A. R. Ives and P. A. Milewski (UW-Madison). We also thank the United States Department of Agriculture-IFAFS (2001-52100-11216 and 2007-02244) for additional support.

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  1. Department of Zoology, UW-Madison, Madison, WI, 53706, USA

    Paul R. Glaum & Anthony R. Ives

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

    David A. Andow

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  1. Paul R. Glaum
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  2. Anthony R. Ives
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  3. David A. Andow
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Correspondence to Anthony R. Ives.

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Glaum, P.R., Ives, A.R. & Andow, D.A. Contamination and management of resistance evolution to high-dose transgenic insecticidal crops. Theor Ecol 5, 195–209 (2012). https://doi.org/10.1007/s12080-010-0109-6

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  • DOI: https://doi.org/10.1007/s12080-010-0109-6

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