Science Insider

The Pesticide Paradox

- November 1, 2020 - Alison McAfee - (excerpt)

pesticide paradox article by Alison McAfee

Other insects have readily developed resistance to pesticides, but honey bees are slow to act

Everywhere we look, from antibiotics to chemotherapies to miticides, we find biological resistance to our attempts at chemical control. Perhaps this phenomenon is most dangerous to us in the world of bacterial infections, where, for example, once-easily-treated pathogens like Staphylococcus aureus can now cause life-threatening illness due to antibiotic resistance.

Crop pests, too, possess this evolutionary superpower — for example, the Colorado potato beetle is resistant to compounds in all major insecticide classes, and cabbage looper caterpillars are increasingly tolerant to Bacillus thuringiensis (Bt) toxin. According to the Arthropod Pesticide Resistance Database, over five hundred species are resistant to insecticides. Which begs the question: If insecticides are such a problem for honey bees, why haven’t they evolved resistance, too?

It is not because honey bees are all equally good at detoxifying pesticides. They aren’t. New research published by Dr. Joe Milone,1 which I was involved in as a collaborating author, shows that different genetic lineages of honey bees vary greatly in both their sensitivity to pesticides and their ability to detoxify them, with some stocks being up to twice as tolerant as others.

“Pesticide resistance is typically seen as a threat to agriculture, from insect pests, but with honey bees and other beneficial insects, tolerance to pesticides can actually be seen as favorable,” says Milone. Milone, now a biologist with the U.S. Environmental Protection Agency, conducted this research in the course of pursuing his doctoral degree. His statements represent his personal opinions and not those of the agency.

Milone tested larvae from eight distinct honey bee stocks to evaluate how well they tolerated a nine-component pesticide cocktail. This blend included insecticides, fungicides, herbicides and acaricides mixed in the same relative proportions as what occurs in the wax of many U.S. commercial honey bee colonies.2

“Screening for pesticide tolerance is generally easiest using adult workers, and previous comparisons of different honey bee populations had tested adults,” says Milone. But, he notes, “Pesticide tolerance can vary between larval and adult life stages.”

Though somewhat sequestered in the wax, the compounds Milone tested can appreciably leach into the brood jelly, which is then gobbled up by the larvae. Milone exposed larvae to the pesticides by rearing them in the laboratory and mixing small amounts of the cocktail in their food, similar to what they might encounter if wax-bound pesticides are desorbed into larval jellies.

Milone investigated a diverse range of stocks, including Russian, Pol-line, Saskatraz, feral, Carniolan (of both the “old world” European genotype and “new world” hybrid genotype) and two geographically isolated Italian stocks. He found that larvae from different lineages tolerated the chemical cocktail to different degrees, with the most tolerant withstanding concentrations twice as high as the least tolerant. What was most surprising, though, was who emerged at the top and bottom of the barrel.

Larvae from the feral colonies tied with old world Carniolans as top-notch survivors. And larvae from Pol-line colonies, a stock carefully selected for varroa-sensitive hygiene and developed at the USDA Bee Laboratory in Baton Rouge, came in dead last. The Russian and Saskatraz larvae — two other putatively varroa-resistant stocks — were in the middle, along with the rest. Milone conducted subsequent experiments demonstrating that pesticide tolerance could largely be explained by the degree of esterase (a type of detoxification enzyme) activity in the larva’s tissue.

This research did not investigate changes in pesticide resistance over time, and the feral source colonies came from a region (the Blue Ridge Mountains of North Carolina) where there should be few opportunities for exposure. So, it is not clear if the feral larvae are so tolerant because they have actually evolved resistance or if they just happened to have been spawned from already-resistant progenitor colonies.

What it does hint at, though, is something that selective breeders and beekeepers have been worried about for a long time: that selection for varroa-resistance traits, as was conducted for the development of the Pol-line, may have inadvertently sacrificed something else. In this case, that “something else” appears to be their tolerance to synthetic chemicals.

“Currently, most honey bee breeding programs are primarily focused on overcoming the challenges posed by the varroa mite,” says Milone. “I feel that varroa poses the greatest immediate threat to apiculture and breeding for varroa tolerance should take priority. That being said, it is important that these selective efforts don’t come at the cost of losing other valuable traits.” Without genetic data and a larger sample, it is hard to say for sure that is what’s going on here, but it is enough to make us think twice about breeding approaches.

What the data do show, unequivocally, is that as far as detoxification ability goes, there is substantial variation in the population. And this kind of variation is the stuff that natural selection acts on. Given a selective pressure, as we might expect environmental pesticides to exert on honey bees, over time the most tolerant colonies should be more likely to survive and occur more frequently in the gene pool. So why aren’t more colonies resistant?

This question has been on the minds of researchers for decades. “Clearly, resistance development has been limited in honey bees when compared with many other insects,” writes the late Dr. Michael James Smirle in his 1988 doctoral thesis.3 “The selection of honey bee strains exhibiting some degree of insecticide resistance would therefore be of considerable benefit to North American Agriculture.”

Smirle, who conducted his research in Dr. Mark Winston’s laboratory at Simon Fraser University, studied the biochemical mechanisms underlying pesticide resistance in honey bees. Among other things, he uncovered that there are not only ….