Effects of Refuge Contamination by Transgenes on Bt Resistance in Pink Bollworm (Lepidoptera: Gelechiidae)

Heuberger, Shannon; Ellers-Kirk, Christa; Yafuso, Christine M.; Gassmann, Aaron J.; Tabashnik, Bruce E.; Dennehy, Timothy J.; Carrière, Yves

doi:10.1093/jee/101.2.504

Cited by 30 publications

(33 citation statements)

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“…The few studies examining feeding behavior of both Bt-susceptible and Bt-resistant insect strains when presented with Bt and non-Bt substrates report little or no differences between the strains in feeding behavior or preference (Schwartz et al 1991, Whalon et al 1993, Harris et al 2006, Heuberger et al 2008. In general, physiological resistance to toxins is expected to evolve more slowly if an insect avoids toxic plants or plant parts because this will reduce selection pressure (Gould and Anderson 1991).…”

Section: Discussionmentioning

confidence: 99%

Adaptation by Western Corn Rootworm (Coleoptera: Chrysomelidae) to Bt Maize: Inheritance, Fitness Costs, and Feeding Preference

et al. 2012

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We examined inheritance of resistance, feeding behavior, and fitness costs for a laboratory-selected strain of western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), with resistance to maize (Zea maize L.) producing the Bacillus thuringiensisBerliner (Bt) toxin Cry3Bb1. The resistant strain developed faster and had increased survival on Bt maize relative to a susceptible strain. Results from reciprocal crosses of the resistant and susceptible strains indicated that inheritance of resistance was nonrecessive. No fitness costs were associated with resistance alleles in the presence of two entomopathogenic nematode species, Steinernema carpocapsae Weiser and Heterorhabditis bacteriophora Poinar. Larval feeding studies indicated that the susceptible and resistant strains did not differ in preference for Bt and non-Bt root tissue in choice assays. KeywordsDiabrotica virgifera virgifera, feeding behavior, pest resistance, transgenic maize RightsWorks produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The content of this document is not copyrighted. ABSTRACT We examined inheritance of resistance, feeding behavior, and Þtness costs for a laboratory-selected strain of western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), with resistance to maize (Zea maize L.) producing the Bacillus thuringiensis Berliner (Bt) toxin Cry3Bb1. The resistant strain developed faster and had increased survival on Bt maize relative to a susceptible strain. Results from reciprocal crosses of the resistant and susceptible strains indicated that inheritance of resistance was nonrecessive. No Þtness costs were associated with resistance alleles in the presence of two entomopathogenic nematode species, Steinernema carpocapsae Weiser and Heterorhabditis bacteriophora Poinar. Larval feeding studies indicated that the susceptible and resistant strains did not differ in preference for Bt and non-Bt root tissue in choice assays.KEY WORDS Diabrotica virgifera virgifera, feeding behavior, pest resistance, transgenic maize

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Section: Discussionmentioning

confidence: 99%

Adaptation by Western Corn Rootworm (Coleoptera: Chrysomelidae) to Bt Maize: Inheritance, Fitness Costs, and Feeding Preference

et al. 2012

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“…Whereas production of F 1 hybrid seeds requires costly hand pollination, self-pollination of F 1 hybrids produces F 2 hybrid seeds (21,22). Crossing Bt cotton with non-Bt cotton creates F 1 hybrids that make Bt toxin and are hemizygous for this trait because they have one copy of the Bt transgene and no corresponding allele (23,24). Self-pollination by such F 1 hybrids creates F 2 hybrid seeds expected to consist of 25% Bt homozygotes and 50% hemizygotes that produce Bt toxin and 25% non-Bt homozygotes that do not (23).…”

Section: Significancementioning

confidence: 99%

“…The seed mixture generated with F 2 hybrids analyzed here may be especially effective against pink bollworm because of the substantial fitness cost associated with its resistance to Cry1Ac and its recessive inheritance of resistance (25), even when feeding on bolls from F 1 hybrids, Cry1Ac-producing bolls from F 2 hybrids (SI Appendix, Table S18), or a mixture of Bt and nonBt seeds (24). Selfing of F 2 plants in subsequent generations is (Fig.…”

Section: Significancementioning

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.

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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“…Production of Bt toxins is dominantly inherited in cotton (Heuberger et al, 2008;Sachs et al, 1998;Zhang et al, 2000). Moreover, Bt cotton varieties marketed in the United States are homozygous for the Bt gene (Adamczyk and Meredith, 2006;Jayaraman, 2005).…”

Section: Origin Of Adventitious Plantsmentioning

confidence: 99%

Outcrossed cottonseed and adventitiousBtplants in Arizona refuges

Heuberger

Yafuso

DeGrandi-Hoffman

et al. 2008

Environ. Biosafety Res.

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Outcrossing of non-Bt cotton (Gossypium hirsutum (L.)) in refuges by transgenic Bt cultivars could reduce the efficacy of refuges for delaying resistance in seed-feeding pests. Based on reports that outcrossing decreased as distance from Bt cotton increased in small-scale studies, we hypothesized that increasing refuge width or distance from Bt fields would reduce outcrossing. In a large-scale study in Arizona, we quantified Bt seed in refuges of experimental and commercial fields, comparing outcrossing between in-field (narrow) and external (wide) refuges and among rows of refuges at various distances from Bt fields. Some refuges, including those in tightly controlled experimental plots, contained up to 8% adventitious Bt plants. Some, but not all, Bt plants likely resulted from Bt seed in the non-Bt seed bags. We did not detect a difference in outcrossing between infield and external refuges. However, statistical power was low because outcrossing was low (< 0.4% of seeds) in both treatments. Higher outcrossing levels (≤ 4.6% of seeds) were observed in the studies measuring outcrossing at various distances from Bt fields, yet outcrossing did not decrease as the distance from Bt fields increased. We hypothesize that Bt plants in refuges cross-pollinated surrounding non-Bt plants, overshadowing the expected association between distance from Bt fields and outcrossing.

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Effects of Refuge Contamination by Transgenes on Bt Resistance in Pink Bollworm (Lepidoptera: Gelechiidae)

Cited by 30 publications

References 0 publications

Adaptation by Western Corn Rootworm (Coleoptera: Chrysomelidae) to Bt Maize: Inheritance, Fitness Costs, and Feeding Preference

Adaptation by Western Corn Rootworm (Coleoptera: Chrysomelidae) to Bt Maize: Inheritance, Fitness Costs, and Feeding Preference

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

Outcrossed cottonseed and adventitiousBtplants in Arizona refuges

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