2513 © The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. Forum Global Patterns of Resistance to Bt Crops Highlighting Pink Bollworm in the United States, China, and India Bruce E. Tabashnik 1,2, and Yves Carrière 1, 1 Department of Entomology, University of Arizona, Tucson, AZ, and 2 Corresponding author, e-mail: brucet@cals.arizona.edu Subject Editor: Aaron Gassmann Received 2 April 2019; Editorial decision 26 May 2019 Abstract Crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt) have advanced pest control, but their benefts have been reduced by evolution of resistance in pests.The global monitoring data reviewed here reveal 19 cases of practical resistance to Bt crops, which is feld-evolved resistance that reduces Bt crop effcacy and has practical consequences for pest control. Each case represents the responses of one pest species in one country to one Bt toxin. The results with pink bollworm (Pectinophora gossypiella) and Bt cotton differ strikingly among the world’s three leading cotton-producing nations. In the southwestern United States, farmers delayed resistance by planting non-Bt cotton refuges from 1996 to 2005, then cooperated in a program that used Bt cotton, mass releases of sterile moths, and other tactics to eradicate this pest from the region. In China, farmers reversed low levels of pink bollworm resistance to Bt cotton by planting second-generation hybrid seeds from crosses between Bt and non-Bt cotton. This approach yields a refuge of 25% non-Bt cotton plants randomly interspersed within felds of Bt cotton. Farmers adopted this tactic voluntarily and unknow- ingly, not to manage resistance, but apparently because of its perceived short-term agronomic and economic benefts. In India, where non-Bt cotton refuges have been scarce and pink bollworm resistance to pyramided Bt cotton producing Cry1Ac and Cry2Ab toxins is widespread, integrated pest management emphasizing short- ening of the cotton season, destruction of crop residues, and other tactics is now essential. Key words: sustainability, resistance management, practical resistance, Pectinophora gossypiella, Bacillus thuringiensis Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) kill some voracious in- sect pests, but are not toxic to most nontarget organisms including natural enemies (Mendelsohn et al. 2003, Romeis et al. 2019). The hectares (ha) planted globally to Bt corn, cotton, and soybean grew from 1.1 million in 1996 to 101 million in 2017 (ISAAA 2017). Bt proteins produced by transgenic crops now include various crystal- line (Cry) proteins (Pardo-López et al. 2013) and a vegetative in- secticidal protein (Vip3Aa; Chakroun et al. 2016). Cry proteins are produced by the bacteria during sporulation and accumulate within cells, whereas Vips are produced during the vegetative phase and secreted (Chakroun et al. 2016). Although Cry proteins and Vip3Aa share a similar mode of action, they have no structural homology, they bind to different sites in the insect midgut, and cross-resistance between them is not strong (Carrière et al. 2015, Chakroun et al. 2016, Tabashnik and Carrière 2017). Bt crops can suppress pests, decrease treatments with conven- tional insecticides, conserve natural enemies, and thereby boost yields and grower profts (Wu et al. 2008, Carpenter 2010, Hutchison et al. 2010, Tabashnik et al. 2010, Edgerton et al. 2012, Kathage and Qaim 2012, NASEM 2016, Dively et al. 2018, Romeis et al. 2019). However, despite the widespread adoption of Bt crop pyramids pro- ducing two or more distinct Bt proteins toxic to each targeted pest (Carrière et al. 2016), evolution of resistance by pests has diminished the benefts of Bt crops (Tabashnik and Carrière 2017). Here we briefy review defnitions of three categories of resist- ance, update the global status of feld-evolved insect resistance to Bt crops, compare resistance to Bt crops with resistance to Bt sprays and conventional insecticides, and summarize the strikingly different responses of the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), to Bt cotton in the United States, China, and India. We conclude that in India, where pink boll- worm resistance to dual-toxin Bt cotton is widespread, integrated pest management (IPM) is now essential for this pest. Each case of published resistance monitoring data reviewed here represents responses of one pest species in one country to one Bt toxin. This updated summary based on a literature review completed on 18 May 2019 considers 44 such cases: 36 cases summarized in a previous review (Tabashnik and Carrière 2017) plus 8 new cases (Fourie et al. 2017, Leite et al. 2017, Smith et al. 2017, Chandrasena et al. 2018, Grimi et al. 2018, Kukanar et al. 2018, Saleem et al. 2019, Vassallo et al. 2019, Yang et al. 2019). We also provide updates Journal of Economic Entomology, 112(6), 2019, 2513–2523 doi: 10.1093/jee/toz173 Advance Access Publication Date: 29 June 2019 Forum Downloaded from https://academic.oup.com/jee/article/112/6/2513/5524246 by guest on 24 May 2022