The pink bollworm, a voracious caterpillar pest, quickly evolved resistance to two Bt proteins produced by biotech cotton in India, but continues to be suppressed in Arizona after more than 20 years. (Alex Yelich/University of Arizona)
Resistance to crops that have been genetically modified to kill pests is surging, according to a study that examines 20 years of data.
In 2016 alone, farmers worldwide planted more than 240 million acres of cotton, corn and soybeans that have been bioengineered to produce insect-killing proteins from the bacterium Bacillus thuringiensis, or Bt.
While Bt proteins have been sprayed on organic farms for more than half a century, some experts worry that widespread use of these proteins in genetically modified crops spurs rapid pest resistance.
To address these concerns, a team of researchers analyzed data on Bt crop use and pest responses from across the world. Their results were published Tuesday in the journal Nature Biotechnology.
“When Bt crops were first introduced in 1996, no one knew how quickly the pests would adapt,” said Bruce Tabashnik, a professor at the University of Arizona. “Now we have a cumulative total of over 2 billion acres of these crops planted during the past two decades and extensive monitoring data, so we can build a scientific understanding of how fast the pests evolve resistance and why.”
The team reviewed published data on 36 cases that shed light on the responses of 15 pest species in 10 nations on every continent except Antarctica. They found resistance dramatically reduced the efficacy of Bt crops in 16 cases as of 2016, up from just three cases in 2005. In these 16 cases, pests developed resistance in about five years on average.
“A silver lining is that in 17 other cases, pests have not evolved resistance to Bt crops,” Tabashnik said, noting that some crops continue to be effective after 20 years.
The remaining three cases are labeled as “early warning of resistance,” in which pest resistance is statistically significant, but not severe enough to produce practical consequences.
“This paper provides us with strong evidence that the
high-dose/refuge strategy for delaying resistance to Bt crops is really working,” said Fred Gould, an entomologist at North Carolina State University and leader of the 2016 National Academy of Sciences study on genetically engineered crops. “This will be critically important information as more crops are engineered to produce Bt toxins.”
The
high-dose/refuge strategy involves bioengineering these crops to produce a high dose of Bt proteins and incorporating refuges that consist of non-Bt plants that pests can eat without exposure to Bt toxins. In theory, planting refuges near Bt crops reduces the likelihood that two resistant insects will mate with each other and improves the chances they will breed with a susceptible mate.
The approach also relies on certain evolutionary principles which have manifested in both the best and worst outcomes the team reviewed, according to the study.
“As expected from evolutionary theory, factors favoring sustained efficacy of Bt crops were recessive inheritance of resistance in pests and abundant refuges,” said Yves Carriere, an entomologist at the University of Arizona.
With recessive inheritance, mating between a susceptible parent and a resistant parent produces offspring that can be killed by the Bt crop.
“Computer models showed that refuges should be especially good for delaying resistance when inheritance of resistance in the pest is recessive,” Carriere said.
The benefits of refuges have been controversial, and the U.S. Environmental Protection Agency has reduced requirements to plant refuges in the United States.
“Perhaps the most compelling evidence that refuges work comes from the pink bollworm, which evolved resistance rapidly to Bt cotton in India, but not in the U.S.,” Tabashnik said.
Farmers in the southwestern United States collaborated with industry, EPA scientists, universities and the U.S. Department of Agriculture to develop an effective refuge strategy. India, on the other hand, also required a refuge strategy, but farmer compliance was low.
“Same pest, same crop, same Bt proteins, but very different outcomes,” Tabashnik said.
The study also reveals that pest resistance to Bt crops is evolving quicker now, largely because resistance to some Bt proteins fosters cross-resistance to related Bt proteins produced by subsequently introduced crops.
An encouraging development, however, is the recent commercialization of biotech crops that produce a novel type of Bt protein known as vegetative insecticidal protein, or Vip. Every other Bt protein in genetically modified crops is a group called crystalline, or Cry, proteins. Since these two groups are so different, cross-resistance between them is low to nonexistent, according to the team.
“This review provides a timely update on the global status of resistance to Bt crops and unique insights that will help to improve resistance management strategies for more sustainable use of Bt crops,” said Yidong Wu, a professor at Nanjing Agricultural University in China.
Tabashnik said the team’s comprehensive evaluation of pest resistance to Bt crops demonstrates how systematic data analyses can be used to enhance understanding and management of resistance.
“These plants have been remarkably useful, and resistance has generally evolved slower than most people expected,” he said. “I see these crops as an increasingly important part of the future of agriculture. The progress made provides motivation to collect more data and to incorporate it in planning future crop deployments.
“We’ve also started exchanging ideas and information with scientists facing related challenges, such as resistance to herbicides in weeds and resistance to drugs in cancer cells.”
Will farmers ever be able to prevent resistance altogether? Tabashnik doesn’t believe so.
“We always expect the pests to adapt,” he said. “However, if we can delay resistance from a few years to a few decades, that’s a big win.”
The research was funded by the USDA.