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

Jin, Lin; Zhang, Haonan; Lu, Yanhui; Yang, Yihua; Wu, Kongming; Tabashnik, Bruce E.; Wu, Yingliang

doi:10.1038/nbt.3100

Cited by 180 publications

(168 citation statements)

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“…The main strategy for delaying pest resistance to Bt crops aims to increase the survival of susceptible insects with "refuges" of host plants that do not produce Bt toxins (9). Although refuges can delay insect adaptation to Bt crops (2,3,9,12), the optimal spatial scale for planting refuges remains unresolved (13)(14)(15). Also, because refuges are often perceived to cause short-term economic sacrifices for growers, they are usually imposed by regulations.…”

mentioning

confidence: 99%

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Wan

Cong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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123

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Extensive cultivation of crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has suppressed some major pests, reduced insecticide sprays, enhanced pest control by natural enemies, and increased grower profits. However, these benefits are being eroded by evolution of resistance in pests. We report a strategy for combating resistance by crossing transgenic Bt plants with conventional non-Bt plants and then crossing the resulting first-generation (F 1 ) hybrid progeny and sowing the second-generation (F 2 ) seeds. This strategy yields a random mixture within fields of three-quarters of plants that produce Bt toxin and one-quarter that does not. We hypothesized that the non-Bt plants in this mixture promote survival of susceptible insects, thereby delaying evolution of resistance. To test this hypothesis, we compared predictions from computer modeling with data monitoring pink bollworm (Pectinophora gossypiella) resistance to Bt toxin Cry1Ac produced by transgenic cotton in an 11-y study at 17 field sites in six provinces of China. The frequency of resistant individuals in the field increased before this strategy was widely deployed and then declined after its widespread adoption boosted the percentage of non-Bt cotton plants in the region. The correspondence between the predicted and observed outcomes implies that this strategy countered evolution of resistance. Despite the increased percentage of non-Bt cotton, suppression of pink bollworm was sustained. Unlike other resistance management tactics that require regulatory intervention, growers adopted this strategy voluntarily, apparently because of advantages that may include better performance as well as lower costs for seeds and insecticides.sustainability | evolution | resistance management | genetically modified | refuge G enetically engineered crops that produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have been planted globally on a cumulative total of over 732 million ha since 1996 (1). The benefits of these Bt crops include pest suppression, reduced insecticide use, enhanced biological control, and increased farmer profits (2-7). However, increasingly rapid evolution of resistance to Bt crops by pests has eroded these benefits (8-11). The main strategy for delaying pest resistance to Bt crops aims to increase the survival of susceptible insects with "refuges" of host plants that do not produce Bt toxins (9). Although refuges can delay insect adaptation to Bt crops (2, 3, 9, 12), the optimal spatial scale for planting refuges remains unresolved (13-15). Also, because refuges are often perceived to cause short-term economic sacrifices for growers, they are usually imposed by regulations.Before 2010, regulations in the United States mandated refuges of non-Bt plants in blocks consisting of separate fields, rows, or strips (14). In 2010, the regulations were modified to include mixtures of Bt and non-Bt seeds generating a random array of Bt and non-Bt plants side by side within...

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confidence: 99%

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Wan

Cong

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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123

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“…Firstly, the amounts of subsidies (direct payments) were postulated as similar for GM crops as for conventional ones. Secondly, the appearance of weeds tolerant to HT plants (Brookes and Barfoot 2013;Green 2014), insect resistance for Bt species, apple scab, or fire blight resistances were not monitored here despite their reported occurrence (Vogt et al 2013;Fahrentrapp et al 2013;Jin et al 2015) but were nonetheless discussed. MCDA and more generally multiattribute models are not directly suitable for time-series evaluation (Bohanec et al 2008).…”

Section: System Boundariesmentioning

confidence: 99%

“…Historically, these aspects have been taken into consideration very early on after Bt toxin release on fields (Tabashnik et al 1994). Resistances from target insects can be overcome (at least temporarily) by using stacking of various toxin variants (13 different Bt proteins have been approved in corn in the USA (Meissle et al 2011;Abbas et al 2013), use of natural refuges (Jin et al 2015), or increase of insecticide spraying. For HT systems, about 44 plant species from at least ten families are reported to be resistant to glyphosate (Green 2014).…”

Section: Distinction Between Short-and Long-term Sustainability Is Crmentioning

confidence: 99%

“…In addition, HT and Bt systems are known to favour less labourintensive crop management allowing less pressure on resources. In particular, Bt systems allow saving of insecticides (quantity used and number of spraying), especially under strong pest pressure and proper crop management, like use of natural refuge strategies (Jin et al 2015 Fig. 7 Hypothetical influence of high acceptance for GM crops on sustainability.…”

Section: Gm Crops Marginally Improve Environmental Sustainabilitymentioning

confidence: 99%

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Genetically modified crops in Switzerland: implications for agrosystem sustainability evidenced by multi-criteria model

Wohlfender-Bühler

Feusthuber

Wager

et al. 2016

Agron. Sustain. Dev.

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In Switzerland, genetically modified (GM) crops have been banned in 2005 and have never been used in agriculture. The relevance and sustainability of genetically modified crops for agrosystems have been assessed following a mandate from the Swiss Parliament defined by the Federal Act on Agriculture (187d al.1). For that, an ex ante study based on a multi-criteria decision analysis model that summarises literature and the opinion of experts has been done.The impacts of genetically modified crops on both environmental and socio-economical sustainability in Switzerland have been assessed. Here, we review four model crops for Swiss agriculture: maize, sugar beet, potato and apple. Each crop was compared for both conventional and genetically modified farming systems that contain a specific trait, namely insecticide production (Bacillus thuringiensis (Bt)), herbicide tolerance (HT), fungal resistance (FR), or bacterial resistance (BR). Results show that six out of seven scenarios showed a lower socio-economical sustainability for genetically modified compared to the conventional systems, whereas a slight improvement in the environmental component, mostly resources use, was observed in all scenarios. In conclusion, our work indicates that only carefully tailored and designed genetically modified crops would meet the high standard of requirements of Swiss agrosystems. Our model has thus allowed a quick diagnostic on the impact of genetically modified cultivation on sustainability.

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“…For modelling purposes, the spatial distribution of Bt and non-Bt plants is considered continuous and random. The proportion of Bt crop in the landscape (ω) is assumed to determine the survival probability (e.g., see Tabashnik et al, 2008;Jin et al, 2015) of the three genotypes (RR, RS and SS): W SS = 1 -ω, W RS = (1 -ω)+h × ω and W RR = 1, where h denotes the dominance of the resistance allele. Spatial spread of a resistance allele under selection was considered under a demogenetic system of deterministic reaction-diffusion equations proposed by Tyutyunov et al (2008) and slightly modified to our purpose (see Supplementary Appendix S1).…”

Section: Theoretical Resistance Spreadmentioning

confidence: 99%

Genetic hitchhiking and resistance evolution to transgenic Bt toxins: insights from the African stalk borer Busseola fusca (Noctuidae)

et al. 2016

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Since transgenic crops expressing Bacillus thuringiensis (Bt) toxins were first released, resistance evolution leading to failure in control of pests populations has been observed in a number of species. Field resistance of the moth Busseola fusca was acknowledged 8 years after Bt maize was introduced in South Africa. Since then, field resistance of this corn borer has been observed at several locations, raising questions about the nature, distribution and dynamics of the resistance trait. Using genetic markers, our study identified four outlier loci clearly associated with resistance. In addition, genetic structure at neutral loci reflected extensive gene flow among populations. A realistically parameterised model suggests that resistance could travel in space at speed of several kilometres a year. Markers at outlier loci delineated a geographic region associated with resistance spread. This was an area of approximately 100 km radius, including the location where resistance was first reported. Controlled crosses corroborated these findings and showed significant differences of progeny survival on Bt plants depending on the origin of the resistant parent. Last, our study suggests diverse resistance mutations, which would explain the widespread occurrence of resistant larvae in Bt fields across the main area of maize production in South Africa.

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

Cited by 180 publications

References 60 publications

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Hybridizing transgenic Bt cotton with non-Bt cotton counters resistance in pink bollworm

Genetically modified crops in Switzerland: implications for agrosystem sustainability evidenced by multi-criteria model

Genetic hitchhiking and resistance evolution to transgenic Bt toxins: insights from the African stalk borer Busseola fusca (Noctuidae)

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