The popular new strategy of planting genetically engineered crops that make two or more toxins to fend off insect pests rests on assumptions that don't always apply, University of Arizona researchers said Thursday, citing the need for improved preventive actions.
The study is published in the Proceedings of the National Academy of Sciences.
Compared with typical insecticide sprays, the Bt toxins produced by genetically engineered crops are much safer for people and the environment, explained Yves Carrière, a professor of entomology in the UA College of Agriculture and Life Sciences who led the study.
Although Bt crops have helped to reduce insecticide sprays, boost crop yields and increase farmer profits, their benefits will be short-lived if pests adapt rapidly, said Bruce Tabashnik, a co-author of the study and head of the UA department of entomology.
"Our goal is to understand how insects evolve resistance so we can develop and implement more sustainable, environmentally friendly pest management," he said.
The recent shift to the "pyramid" strategy – inclusion of more than one toxin – to thwart further evolution of pest resistance to Bt crops will expedite resistance, researchers say.
As reported in the study, the pyramid strategy has been adopted extensively, with two-toxin Bt cotton, for example, completely replacing one-toxin Bt cotton since 2011 in the U.S.
Though many scientists agree two-toxin plants are more durable, the extent of the advantage of the pyramid strategy, however, rests on assumptions that are not always met. Using lab experiments, computer simulations and analysis of published experimental data, researchers say the new results help explain why one major pest has started to become resistant faster than anticipated.
"The pyramid strategy has been touted mostly on the basis of simulation models," said Carrière. "We tested the underlying assumptions of the models in lab experiments with a major pest of corn and cotton. The results provide empirical data that can help to improve the models and make the crops more durable."
One critical assumption of the pyramid strategy is that the crops provide redundant killing, Carrière explained.
"Redundant killing can be achieved by plants producing two toxins that act in different ways to kill the same pest," he said, "so, if an individual pest has resistance to one toxin, the other toxin will kill it."
In the real world, things are a bit more complicated, Carrière's team found out. Thierry Brévault, a visiting scientist from France, led the lab experiments at the UA. His home institution, the Center for Agricultural Research for Development, or CIRAD, is keenly interested in factors that could affect pest resistance to Bt crops in Africa.
"We obviously can't release resistant insects into the field, so we breed them in the lab and bring in the crop plants to do feeding experiments," Carrière said. For their experiments, the group collected cotton bollworm – also known as corn earworm or Helicoverpa zea –, a species of moth that is a major agricultural pest, and selected it for resistance against one of the Bt toxins, Cry1Ac.
As expected, the resistant caterpillars survived after munching on cotton plants producing only that toxin. The surprise came when Carrière's team put them on pyramided Bt cotton containing Cry2Ab in addition to Cry1Ac.
If the assumption of redundant killing is correct, caterpillars resistant to the first toxin should survive on one-toxin plants, but not on two-toxin plants, because the second toxin should kill them, Carrière explained.
"But on the two-toxin plants, the caterpillars selected for resistance to one toxin survived significantly better than caterpillars from a susceptible strain."
These findings show that the crucial assumption of redundant killing does not apply in this case and may also explain the reports indicating some field populations of cotton bollworm rapidly evolved resistance to both toxins, researchers say.
Moreover, the team's analysis of published data from eight species of pests reveals that some degree of cross-resistance between Cry1 and Cry2 toxins occurred in 19 of 21 experiments. Contradicting the concept of redundant killing, cross-resistance means that selection with one toxin increases resistance to the other toxin.
According to the study's authors, even low levels of cross-resistance can reduce redundant killing and undermine the pyramid strategy. Carrière explained that this is especially problematic with cotton bollworm and some other pests that are not highly susceptible to Bt toxins to begin with.
The team found violations of other assumptions required for optimal success of the pyramid strategy. In particular, inheritance of resistance to plants producing only Bt toxin Cry1Ac was dominant, which is expected to reduce the ability of refuges to delay resistance.
Under ideal conditions, inheritance of resistance is not dominant and the susceptible pests emerging from refuges greatly outnumber the resistant pests. If so, the matings between two resistant pests needed to produce resistant offspring are unlikely. But if inheritance of resistance is dominant, as seen with cotton bollworm, matings between a resistant moth and a susceptible moth can produce resistant offspring, which hastens resistance, researchers found.
According to Tabashnik, optimistic assumptions have led the EPA to greatly reduce requirements for planting refuges to slow evolution of pest resistance to two-toxin Bt crops.
This should lead to consideration of larger refuges to push resistance further into the future, Carrière said.
"Our simulations tell us that with 10% of acreage set aside for refuges, resistance evolves quite fast, but if you put 30% or 40% aside, you can substantially delay it."
"Our main message is to be more cautious, especially with a pest like the cotton bollworm," Carrière said. "We need more empirical data to refine our simulation models, optimize our strategies and really know how much refuge area is required. Meanwhile, let's not assume that the pyramid strategy is a silver bullet."
Source: University of Arizona