Genetically engineered crops that produce insecticidal toxins from Bacillus thuringiensis (Bt) are grown widely for pest control. However, insect adaptation can reduce the toxins' efficacy. The predominant strategy for delaying pest resistance to Bt crops requires refuges of non-Bt host plants to provide susceptible insects to mate with resistant insects. Variable farmer compliance is one of the limitations of this approach. Here we report the benefits of an alternative strategy where sterile insects are released to mate with resistant insects and refuges are scarce or absent. Computer simulations show that this approach works in principle against pests with recessive or dominant inheritance of resistance. During a large-scale, four-year field deployment of this strategy in Arizona, resistance of pink bollworm (Pectinophora gossypiella) to Bt cotton did not increase. A multitactic eradication program that included the release of sterile moths reduced pink bollworm abundance by >99%, while eliminating insecticide sprays against this key invasive pest.
The pink bollworm, Pectinophora gossypiella, is a world-wide pest of cultivated cotton. In certain growing regions populations are suppressed by a sterile release strategy. Efforts to improve the sterile insect technique as well as our understanding of lepidopteran biology could benefit greatly from a germ-line transformation system. We report transformation of pink bollworm with a piggyBac transposable element carrying the enhanced green flourescent protein (EGFP) marker gene. This vector-marker system resulted in recovery of transgenics at a rate of approximately 3.5%. Integration of the transforming construct that was typical of piggyBac was demonstrated by Southern analysis and sequence determination of transposon flanks. Expression of the EGFP marker was visualized by fluorescent microscopy and Western Blot analysis. Maintenance of transformed strains indicates that the transgene segregates in a Mendelian fashion and has been stable over fourteen generations to date.
Invasive organisms pose a global threat and are exceptionally difficult to eradicate after they become abundant in their new habitats. We report a successful multitactic strategy for combating the pink bollworm (Pectinophora gossypiella), one of the world’s most invasive pests. A coordinated program in the southwestern United States and northern Mexico included releases of billions of sterile pink bollworm moths from airplanes and planting of cotton engineered to produce insecticidal proteins from the bacteriumBacillus thuringiensis(Bt). An analysis of computer simulations and 21 y of field data from Arizona demonstrate that the transgenic Bt cotton and sterile insect releases interacted synergistically to reduce the pest’s population size. In Arizona, the program started in 2006 and decreased the pest’s estimated statewide population size from over 2 billion in 2005 to zero in 2013. Complementary regional efforts eradicated this pest throughout the cotton-growing areas of the continental United States and northern Mexico a century after it had invaded both countries. The removal of this pest saved farmers in the United States $192 million from 2014 to 2019. It also eliminated the environmental and safety hazards associated with insecticide sprays that had previously targeted the pink bollworm and facilitated an 82% reduction in insecticides used against all cotton pests in Arizona. The economic and social benefits achieved demonstrate the advantages of using agricultural biotechnology in concert with classical pest control tactics.
Pest insects harm crops, livestock and human health, either directly or by acting as vectors of disease. The Sterile Insect Technique (SIT) – mass-release of sterile insects to mate with, and thereby control, their wild counterparts – has been used successfully for decades to control several pest species, including pink bollworm, a lepidopteran pest of cotton. Although it has been suggested that genetic engineering of pest insects provides potential improvements, there is uncertainty regarding its impact on their field performance. Discrimination between released and wild moths caught in monitoring traps is essential for estimating wild population levels. To address concerns about the reliability of current marking methods, we developed a genetically engineered strain of pink bollworm with a heritable fluorescent marker, to improve discrimination of sterile from wild moths. Here, we report the results of field trials showing that this engineered strain performed well under field conditions. Our data show that attributes critical to SIT in the field – ability to find a mate and to initiate copulation, as well as dispersal and persistence in the release area – were comparable between the genetically engineered strain and a standard strain. To our knowledge, these represent the first open-field experiments with a genetically engineered insect. The results described here provide encouragement for the genetic control of insect pests.
Evolution of resistance by pests can reduce the benefits of transgenic crops that produce toxins from Bacillus thuringiensis (Bt) for insect control. One of the world's most important cotton pests, pink bollworm (Pectinophora gossypiella), has been targeted for control by transgenic cotton producing Bt toxin Cry1Ac in several countries for more than a decade. In China, the frequency of resistance to Cry1Ac has increased, but control failures have not been reported. In western India, pink bollworm resistance to Cry1Ac has caused widespread control failures of Bt cotton. By contrast, in the state of Arizona in the southwestern United States, monitoring data from bioassays and DNA screening demonstrate sustained susceptibility to Cry1Ac for 16 y. From 1996-2005, the main factors that delayed resistance in Arizona appear to be abundant refuges of non-Bt cotton, recessive inheritance of resistance, fitness costs associated with resistance and incomplete resistance. From 2006-2011, refuge abundance was greatly reduced in Arizona, while mass releases of sterile pink bollworm moths were made to delay resistance as part of a multi-tactic eradication program. Sustained susceptibility of pink bollworm to Bt cotton in Arizona has provided a cornerstone for the pink bollworm eradication program and for integrated pest management in cotton. Reduced insecticide use against pink bollworm and other cotton pests has yielded economic benefits for growers, as well as broad environmental and health benefits. We encourage increased efforts to combine Bt crops with other tactics in integrated pest management programs.
The mechanisms by which the application of formulated pheromone interferes with mating in the pink bollworm moth (PBW), Pectinophora gossypiella were examined in 0.4 ha cotton fields using high-dose (78 mg A.I.) sealed polyethylene dispensers. Walk-in, field wind tunnels 6.2 m long were placed over two rows of cotton. Treatments consisted of a control, a tunnel in a field free of disruptant formulation; a 3-rope treatment, in which the field was free of pheromone but one of the cotton rows in the wind tunnel was treated with 3 PBW ropes; and a rope-grid treatment, in which the field was treated with PBW ropes at the standard density of 1000 ha −1 and one of the cotton rows inside the wind tunnel was treated with 3 PBW ropes. We released marked males into the tunnels near sunset or held them in field cages for 24 h prior to assay. Two pheromone traps at the tunnel's upwind end monitored the ability of males to locate point sources of pheromone. In the 3-rope tunnel, traps placed upwind of the cotton row treated with disruptant pheromone captured far fewer males than those placed upwind of the untreated cotton row. In the tunnel situated in the centre of the rope-gridded field, very few males were caught in traps in both rows, indicating a camouflage of the pheromone plumes from the traps by the background of airborne disruptant drawn into the tunnel from the field. Activity of moths near the synthetic pheromone sources was video-recorded. Males oriented to, landed on or near, and walked on or near, PBW ropes, indicating competition between pheromone sources as a mechanism of mating disruption. Most males visiting PBW ropes became quiescent or disappeared from the field of view after a few minutes, suggesting a habituation/adaptation of response. The rhythm of attraction of males held in the field for 24 h before release was comprised of a small peak of activity near 2000 h, with the majority of attraction between 2300 and 0300 h. Much of the attraction before 0100 appears to be an advancement of the male's normal diel rhythm, caused by the presence of disruptant. Together these findings indicate that mating disruption of pink bollworm using the PBW ropes is achieved by a combination of mechanisms: a camouflage of natural plumes, competition between pheromone sources, habituation, and some advancement of the male's rhythm of response.
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