Cultivation of transgenic crops engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt) has grown rapidly in the past 25 years. Bt crops have had noteworthy successes, but resistance to Bt crops has evolved in numerous instances. Five cases of practical resistance to Bt proteins that are produced by transgenic crops are documented for corn earworm (Helicoverpa zea), which is the most for any pest. (Photo by John C. French Sr., Retired, Universities:Auburn, GA, Clemson and U of MO, Bugwood.org)

By John P. Roche, Ph.D.

Insect pests damaging crops is a huge problem worldwide, threatening food security and causing significant economic loss. One avenue to address this is to genetically engineer crops to produce proteins from the bacterium Bacillus thuringiensis (Bt) that kill pests but are safe for most nontarget organisms. Although Bt-modified crops have been useful for controlling pests in numerous instances, some pests evolve resistance to Bt insecticide proteins. Therefore, scientists must evaluate the efficacy of Bt modified crops and find ways to delay evolution of insecticide resistance.

Sustained susceptibility to Bt cotton was essential for eradicating the pink bollworm (Pectinophora gossypiella) from the United States and Mexico, which it had invaded more than a century ago.As part of a multi-tactic program, pink bollworm caterpillars were mass reared (as shown here) and 11 billion sterile moths were released by airplanes to overwhelm its populations in the field. By contrast, this pest evolved resistance to dual-toxin Bt cotton in India, where it was used extensively with scarce non-Bt host plant refuges and limited integration of other tactics. (Photo by Alexander Yelich, University of Arizona)

In a review published in January in the Journal of Economic Entomology, Bruce Tabashnik, Ph.D., and Yves Carrière, Ph.D., of the University of Arizona and Jeffrey Fabrick, Ph.D., of the USDA Agricultural Research Service analyze both of these needs by examining patterns of Bt resistance in agricultural pests around the globe. The review is part of a special collection on field-evolved resistance to Bt crops.

The acreage of Bt-modified crops has grown rapidly in the past 20 years, with over a 100-fold increase between 1996 and 2019. The USDA estimates that, in the U.S. from 2009 to 2020, Bt crops accounted for more than 75 percent of the area planted with corn and cotton and that, from 2016 to 2020, 81 percent of corn and 87 percent of cotton planted in the U.S. was engineered to produce Bt proteins.

Bt crops have helped to suppress pests while also decreasing the need for conventional insecticides and augmenting the effectiveness of biological control species. “Two stunning successes of Bt crops against invasive pests in the United States,” Tabashnik says, “are suppression of the European corn borer (Ostrinia nubilalis) to its lowest levels in more than 75 years by Bt corn and eradication of the pink bollworm (Pectinophora gossypiella) using Bt cotton together with sterile moth releases and other tactics.” An example of a success against a native pest is the control of the tobacco budworm moth Chloridea virescens using Bt cotton in the U.S. and Mexico.

In their review, Tabashnik, Carrière, and Fabrick examined 73 sets of data on monitoring resistance to Bt crops, including information about responses to 10 Bt toxins in 22 species of moth and two species of beetle. They differentiated resistance found in these studies into the following three categories:

1. practical resistance, in which more than half of the individuals in a population are resistant and the field efficacy of the Bt crop has decreased;
2. early warning of resistance, in which resistance has evolved but fewer than half of individuals are resistant and efficacy of the Bt crop has not decreased;
3. no decrease in susceptibility, in which there is no statistically significant decrease observed in susceptibility.

In the 73 data sets examined, they found 26 cases of practical resistance. The average time from first planting of a particular Bt crop to the appearance of practical resistance was 6.6 years. Over half of the cases of practical resistance were in three species—the moths Helicoverpa zea and Spodoptera frugiperda and the beetle Diabrotica virgifera virgifera. Geographically, half of the instances of practical resistance were in the U.S. This makes sense, as the U.S. has planted Bt crops widely and extensively monitored resistance.

Tabashnik and colleagues found 17 instances of early warning of resistance. The mean time of detection of early warning of resistance was 8.6 years after exposure to Bt crops.

Thirty instances of no significant resistance were found after two to 24 years of exposure, with an average duration since exposure to Bt crops of 12.2 years.

The many instances of practical resistance lead to the question of how resistance can be delayed or prevented. One important way to reduce resistance is by creating refuges consisting of non-Bt-modified plants that serve as hosts for pest insects that are not resistant. Refuges were first envisioned to reduce evolution of resistance to insecticide sprays, but they have been crucial for slowing evolution of resistance to Bt insecticides. Because the refuge plants don’t produce Bt proteins, they allow survival of susceptible insects that can mate with any resistant insects that emerge from Bt crops.

Another factor that can hinder the evolution of resistance is increasing the concentration of Bt proteins enough to kill insects that are heterozygous for resistance, i.e., they carry only one allele that confers resistance. This “high-dose” strategy makes the resistance functionally recessive and less likely to spread quickly.

Bruce Tabashnik, Ph.D., regents professor and head of the Department of Entomology at the University of Arizona, (shown here in a strict quarantine lab holding a container lid with pink bollworm pupae and prepupae). (Photo courtesy of Arizona Daily Star; republished with permission. Photo may not be republished or disseminated without permission of the Arizona Daily Star.)

Yves Carrière, Ph.D., professor, Department of Entomology, University of Arizona. (Photo by Lara Herrington Watson)

Jeffrey Fabrick, Ph.D., research entomologist, USDA Agricultural Research Service, U.S. Arid Land Agricultural Research Center, Maricopa, Arizona.

Tabashnik says, “Theory and empirical evidence indicate that recessive inheritance of pest resistance to Bt crops and abundant refuges of non-Bt host plants can help to sustain the efficacy of Bt crops. When inheritance of resistance is not recessive, the abundance of refuges relative to Bt crops can be increased to effectively delay evolution of resistance.”

Strategies being explored to heighten the efficacy of Bt crops include targeting each pest with two or more Bt proteins and using Bt proteins together with RNA interference (RNAi) insecticides. In the close of their review, Tabashnik and colleagues emphasize that rather than relying on any one control tactic—such as transgenic crops—sustainable pest suppression combines diverse integrated pest management tools.

John P. Roche, Ph.D., is an author, biologist, and science writer with a Ph.D. in the biological sciences and a dedication to making rigorous science clear and accessible. He writes books and articles, and provides writing for universities, scientific societies, and publishers. Professional experience includes serving as a scientist and scientific writer at Indiana University, Boston College, and the University of Massachusetts Medical School, and as editor-in-chief of science periodicals at Indiana University and Boston College.