Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops

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The ‘natural refuge strategy” for delaying insect resistance to transgenic cotton that produces insecticidal proteins from Bacillus thuringiensis (Bt) relies on refuges of host plants other than cotton that do not make Bt toxins. We tested this widely adopted strategy by comparing predictions from modeling with data from a four-year field study of cotton bollworm (Helicoverpa armigera) resistance to transgenic cotton producing Bt toxin Cry1Ac in six provinces of northern China. Bioassay data revealed that the percentage of resistant insects increased from 0.93% in 2010 to 5.5% in 2013. Modeling predicted that the percentage of resistant insects would exceed 98% in 2013 without natural refuges, but would increase to only 1.1% if natural refuges were as effective as non-Bt cotton refuges. Therefore, the results imply that natural refuges delayed resistance, but were not as effective as an equivalent area of non-Bt cotton refuges. The percentage of resistant insects with nonrecessive inheritance of resistance increased from 37% in 2010 to 84% in 2013. Switching to Bt cotton producing two or more toxins and integrating other control tactics could slow further increases in resistance.

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Figure 1: Computer simulations of the effect of natural refuges and dominance on evolution of resistance to Bt cotton by H. armigera in northern China.
Figure 2: Computer simulations of the effect of refuge percentage on evolution of resistance to Bt cotton by H. armigera in northern China.
Figure 3: Observed versus predicted evolution of resistance to Bt cotton by H. armigera in northern China.
Figure 4: Survival at a diagnostic concentration of Cry1Ac for F1 progeny of H. armigera from 17 sites in six provinces of northern China.
Figure 5: Experimental design for estimating the percentage of resistant individuals with nonrecessive resistance.
Figure 6: Performance on Bt cotton plants of H. armigera from a susceptible strain (SCD), a resistant strain derived from a field-selected population in northern China (AY), and their F1 progeny (AY × SCD).


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We thank M. Sisterson and three anonymous reviewers for their comments that improved the manuscript. This work was funded by grants from the Ministry of Agriculture of China (2014ZX08012-004), the National Natural Science Foundation of China (31071983 and 31321004), the 111 program of China (B07030) and the US Department of Agriculture Biotechnology Risk Assessment Grants program (2011-33522-30729). We thank M.P. Carey (Case Western Reserve University, USA) for providing activated Cry1Ac toxin.

Author information

Y.W., K.W., Y.Y. and B.E.T. contributed to research design; L.J., H.Z. and Y.L. conducted experiments; B.E.T. conducted computer simulations; Y.W., B.E.T., K.W., L.J. and Y.Y. analyzed data. Y.W. and B.E.T. wrote the paper. All authors discussed the results and commented on the manuscript.

Correspondence to Yidong Wu.

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Competing interests

B.E.T. is coauthor of a patent on modified Bt toxins, “Suppression of Resistance in Insects to Bacillus thuringiensis Cry Toxins, Using Toxins that do not Require the Cadherin Receptor” (patent numbers: CA2690188A1, CN101730712A, EP2184293A2, EP2184293A4, EP2184293B1, WO2008150150A2, WO2008150150A3). Pioneer, Dow AgroSciences, Monsanto and Bayer CropScience did not provide funding to support this work, but may be affected financially by publication of this paper and have funded other work by B.E.T.

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Jin, L., Zhang, H., Lu, Y. et al. Large-scale test of the natural refuge strategy for delaying insect resistance to transgenic Bt crops. Nat Biotechnol 33, 169–174 (2015) doi:10.1038/nbt.3100

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