Transgenic crops have revolutionized insect pest control, but their effectiveness has been reduced by evolution of resistance in pests. We analyzed global monitoring data reported during the first two decades of transgenic crops, with each case representing the responses of one pest species in one country to one insecticidal protein from Bacillus thuringiensis (Bt). The cases of pest resistance to Bt crystalline (Cry) proteins produced by transgenic crops increased from 3 in 2005 to 16 in 2016. By contrast, in 17 other cases there was no decrease in pest susceptibility to Bt crops, including the recently introduced transgenic corn that produces a Bt vegetative insecticidal protein (Vip). Recessive inheritance of pest resistance has favored sustained susceptibility, but even when inheritance is not recessive, abundant refuges of non-Bt host plants have substantially delayed resistance. These insights may inform resistance management strategies to increase the durability of current and future transgenic crops.

Surge in insect resistance to transgenic crops and prospects for sustainability.

Transgenic crops producing Bacillus thuringiensis (Bt) toxins are used worldwide to control major pests of corn and cotton. Development of strategies to delay the evolution of pest resistance to Bt crops requires an understanding of factors affecting responses to natural selection, which include variation in survival on Bt crops, heritability of resistance, and fitness advantages associated with resistance mutations. The two main strategies adopted for delaying resistance are the refuge and pyramid strategies. Both can reduce heritability of resistance, but pyramids can also delay resistance by reducing genetic variation for resistance. Seasonal declines in the concentration of Bt toxins in transgenic cultivars, however, can increase the heritability of resistance. The fitness advantages associated with resistance mutations can be reduced by agronomic practices, including increasing refuge size, manipulating refuges to increase fitness costs, and manipulating Bt cultivars to reduce fitness of resistant individuals. Manipulating costs and fitness of resistant individuals on transgenic insecticidal crops may be especially important for thwarting evolution of resistance in haplodiploid and parthenogenetic pests. Field-evolved resistance to Bt crops in only five pests during the last 14 years suggests that the refuge strategy has successfully delayed resistance, but the accumulation of resistant pests could accelerate.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1752-4571.2010.00129.x

Evolutionary ecology of insect adaptation to Bt crops

The quantitative levels of CrylAc and the seasonal decline in expression differed significantly among the eight commercial Bollgard hybrids tested. The CrylAc expression was found to be variable among the hybrids and alsobetween different plant parts. The leaves of Bt-cotton plants were found to have the highest levels of CrylAc expression followed by squares, bolls and flowers. The toxin expression in the boll-rind, square bud and ovary of flowers was clearly inadequate to confer full protection to the fruiting parts. Increasing levels of Helicoverpa armigera survival were correlated with the toxin levels decreasing below 1.8 μg/g in the plant parts. Genotype-independent seasonal decline of the CrylAc toxin levels was observed in all the hybrids. CrylAc expression decreased consistently as the plant aged. The decline in CrylAc was more rapid in some hybrids compared to others. The choice of parental background appeared to be crucial for sustainable expression of the crylAc transgene. The implications of variability in CrylAc expression and the seasonal decline on bollworm management are discussed.

Temporal and intra-plant variability of Cry1Ac expression in Bt-cotton and its influence on the survival of the cotton bollworm, Helicoverpa armigera(Hubner) (Noctuidae: Lepidoptera)

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) also known as spotted-wing drosophila (SWD), is a pest native to Southeast Asia. In the last few decades, the pest has expanded its range to affect all major European and American fruit production regions. SWD is a highly adaptive insect that is able to disperse, survive, and flourish under a range of environmental conditions. Infestation by SWD generates both direct and indirect economic impacts through yield losses, shorter shelf life of infested fruit, and increased production costs. Fresh markets, frozen berries, and fruit export programs have been impacted by the pest due to zero tolerance for fruit infestation. As SWD control programs rely heavily on insecticides, exceedance of maximum residue levels (MRLs) has also resulted in crop rejections. The economic impact of SWD has been particularly severe for organic operations, mainly due to the limited availability of effective insecticides. Integrated pest management (IPM) of SWD could significantly reduce chemical inputs but would require substantial changes to horticultural management practices. This review evaluates the most promising methods studied as part of an IPM strategy against SWD across the world. For each of the considered techniques, the effectiveness, impact, sustainability, and stage of development are discussed.

Drosophila suzukii (Diptera: Drosophilidae): A Decade of Research Towards a Sustainable Integrated Pest Management Program

The insertion of genes encoding insecticidal Cry1A delta-endotoxins from the bacterium Bacillus thuringiensis Berliner variety kurstaki (Bt) into varieties of cotton (Gossypium spp.) was undertaken to assist in the control of a range of lepidopteran pests. In Australia, where Helicoverpa armigera (Hubner) and Helicoverpa punctigera (Wallengren) are major pests, the level of control is useful, but not complete, because efficacy declines as the crop matures. Fluctuations in the efficacy of Bt cotton, to the extent that some insects survive, provide opportunities for H. armigera to develop resistance to the Bt toxin. Therefore, variations in the efficacy of Bt cotton need to be understood if we are to plan rational resistance management strategies to retard the rate of the development of resistance. We measured the changes in efficacy associated with plant development over the growing season, in the field and glasshouse. In addition, the levels of Cry1Ac protein toxin and cry1Ac RNA were determined. In this first demonstration of the relationship between these three factors, we found that the developmental decline in bioefficacy in field-grown plants was associated with reduced cry1Ac transcript levels and Bt toxin levels in postsquaring cotton. In addition, changes in plant chemistry associated with the maturation of the cotton plant were observed to contribute to changes in the efficacy of Bt toxin. Results from the field and glasshouse suggested that variations in efficacy within the growing season and between seasons also may be influenced by environmental factors.

https://bioone.org/journals/Journal-of-Economic-Entomology/volume-98/issue-3/0022-0493-98.3.1007/Season-Long-Variation-in-Expression-of-Cry1Ac-Gene-and-Efficacy/10.1603/0022-0493-98.3.1007.pdf

Season-long variation in expression of Cry1Ac gene and efficacy of Bacillus thuringiensis toxin in transgenic cotton against Helicoverpa armigera (Lepidoptera: Noctuidae).

We report on the efficacy of 0.5 M (61,000 ppm) erythritol (E) in Truvia Baking Blend, 10 ppm lufenuron (L), and their combination (LE) to reduce egg and larval densities of wild populations of Drosophila suzukii (Matsumura) infesting fields of rabbiteye blueberries (Vaccinium virgatum) and blackberries (Rubus sp.). Formulations included the active ingredients (lufenuron, erythritol, or both), sugar (in control and erythritol treatments), and Dawn hand-soap applied to plants with pressurized 3-gallon garden spray tanks. The three chemical treatments (E, L, and LE) had no effect on D. suzukii ovipositing in blackberry and blueberry fruit, but they did reduce larval infestation by 75%, particularly densities of first and second instars. Erythritol and lufenuron were equally efficacious compounds as a D. suzukii ovicide and larvicide, but they did not display additive or synergistic activity. Extremely high larval mortality in control fruits show an age structure heavily skewed toward egg output.

Erythritol and Lufenuron Detrimentally Alter Age Structure of Wild Drosophila suzukii (Diptera: Drosophilidae) Populations in Blueberry and Blackberry.

Field cage experiments were conducted to determine the impact of bollworms, Helicoverpa zea (Boddie), on yields of Bollgard II and Widestrike cotton, Gossypium hirsutum L. One-day-old bollworm larvae were infested in white flowers of Bollgard II and in white flowers and terminals of Widestrike cotton. The infestation levels included 0, 50, and 100% of white flowers for each type of cotton. Terminal infestations included one or two larvae per terminal on Widestrike cotton. Larvae were placed in flowers of Bollgard II cotton each day for 1 to 4 wk during the first 4 wk of flowering during 2003, 2004, and 2005 seasons and in the flowers or terminals of Widestrike cotton each day for 1 to 3 wk. Averaged across years and durations of infestation, yields of Bollgard II cotton were significantly reduced compared with noninfested Bollgard II cotton when 100% of white flowers were infested. For Widestrike cotton, there was a reduction in yield when 100% of white flowers were infested in 2005, but not in 2006. There was a significant relationship for cumulative numbers of white flowers infested on seedcotton yield of Bollgard II during one of the 3 yr of the experiment. The regression equation during that year had a slope of −0.77. No significant relationships were observed for cumulative numbers of white flowers infested on yields of Widestrike cotton. Results of the current experiment suggest bollworms will rarely cause yield losses of Bollgard II and Widestrike cotton. Future research will need to focus on developing specific thresholds for bollworms on Bollgard II and Widestrike cotton.

Yield response of dual-toxin Bt cotton to Helicoverpa zea infestations.

The verde plant bug, Creontiades signatus (Distant), has been present in south Texas for several years but has more recently been documented as an economic threat to cultivated cotton, Gossypium hirsutum L. Our studies over 2 yr (2009 and 2010) and two locations (Weslaco and Corpus Christi, TX) investigated feeding-injury of the verde plant bug to a range of cotton boll age classes defined by boll diameter and accumulated degree-days (anthesis to the time of infesting) for first-position cotton bolls infested with the plant bugs. The most detrimental damage to younger cotton bolls from verde plant bug feeding was boll abscission. Cotton bolls <04 accumulating daily degree-days (ACDD), or a boll diameter of 1.3 cm were subject to 60–70% higher boll abscission when compared with the noninfested controls. Significantly higher boll abscission occurred from verde plant bug injured bolls compared with the controls up to 162 ACDD or a mean boll diameter 2.0 cm. Cotton seed weights were significantly reduced up to 179 ACDD or a boll diameter of 2.0 cm at Weslaco in 2009, and up to 317 ACDD or boll diameter 2.6 cm for Weslaco in 2010 when compared with the noninfested controls. Lint weight per cotton boll for infested and noninfested bolls was significantly reduced up to 262 ACDD or boll diameter 2.5 for Corpus Christi in 2010 and up to 288 ACCD or boll diameter 2.6 cm for Weslaco, TX, in 2010. Damage ratings (dependant variable) regressed against infested and noninfested seed-cotton weights showed that in every instance, the infested cotton bolls had a strong and significant relationship with damage ratings for all age classes of bolls. Damage ratings for the infested cotton bolls that did not abscise by harvest showed visual signs of verde plant bug feeding injury and the subsequent development of boll rot; however, these two forms of injury causing lint and seed mass loss are hard to differentiate from open or boll-locked cotton bolls. Based on the results of both lint and seed loss over 2 yr and four studies cotton bolls should be protected up to ≈300 ACDD or a boll diameter of 2.5 cm. This equilibrates to bolls that are 12–14 d of age dependent upon daily maximum and minimum temperatures.

Verde plant bug (Hemiptera: Miridae) feeding injury to cotton bolls characterized by boll age, size, and damage ratings.

Quantification of CryIA(c) δ-endotoxin in transgenic Bt cotton: correlating insect survival to different protein levels among plant parts and varieties.

Studies during the past 5 yr have shown that the overall level of protein (Cry1Ac) produced from the cry1Ac transgene (Monsanto Co., St. Louis, MO) differ among commercial Bollgard cotton, Gossypium hirsutum L., cultivars. These differences between cultivars are under genetic control and have been correlated with efficacy of certain lepidopteran pests. Previous studies have shown that the parental background (i.e., non-Cry1Ac conventional cultivar) has a significant influence on the amount of Cry1Ac protein in Bollgard cultivars. Unlike the backcross technique commonly used to acquire commercial Bollgard cultivars, we used forward breeding to obtain cultivars of Bollgard cotton that were selected for various levels of Cry1Ac. These differences in the amount of Cry1Ac were correlated with growth and survival of two lepidopteran pests of cotton. Implications for effective resistance management as well as relative ease of this procedure are discussed.

Selecting for Efficacy of Bollgard Cotton Cultivars Against Various Lepidoptera Using Forward Breeding Techniques

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