Differences in larval pesticide tolerance and esterase activity across honey bee (Apis mellifera) stocks

Authors: MILONE, JOSEPH - North Carolina State University; Rinkevich, Frank; MCAFEE, ALISON - North Carolina State University; FOSTER, LEONARD - University Of British Columbia; TARPY, DAVID - North Carolina State University

Submitted to: Ecotoxicology and Environmental Safety
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/13/2020
Publication Date: 9/2/2020
Citation: Milone, J.P., Rinkevich Jr, F.D., McAfee, A., Foster, L.J., Tarpy, D. 2020. Differences in larval pesticide tolerance and esterase activity across honey bee (Apis mellifera) stocks. Ecotoxicology and Environmental Safety. 206:111213. https://doi.org/10.1016/j.ecoenv.2020.111213.
DOI: https://doi.org/10.1016/j.ecoenv.2020.111213

Interpretive Summary: Honey bees are genetically diverse and are propagated on a continuum of free-range open mating to highly controlled closed mating selective breeding programs. We tested the pesticide sensitivity to stocks of honey bees that fall on this continuum. Generally, the stocks with the least controlled mating regimes had the lowest pesticide sensitivity while those that were selectively bred were the most sensitive. The sensitivity was due to different quantities and qualities of esterase detoxification enzyme activities where the least sensitive stocks had the highest and most resilient activity. This suggests that selective breeding may have unintended consequences and that genetic variation exists in honey bee stocks that may be exploited for selection for reduced pesticide sensitivity.

Technical Abstract: Honey bee populations in North America are an amalgamation of diverse progenitor ecotypes experiencing varying levels of artificial selection. Genetic differences between populations can result in variable susceptibility towards environmental stressors, and here we compared pesticide tolerances across breeding stocks using a mixture of seven pesticides frequently found in colonies providing pollination services. We administered the pesticide mixture chronically to in vitro reared larvae at four concentrations of increasing Hazard Quotient (HQ, or cumulative toxicity) and measured mortality during larval development. We found that different stocks had significantly different tolerances to our pesticide mixture as indicated by their median lethal toxicity (HQ50). The intensively selected Pol-Line stock exhibited the greatest pesticide sensitivity while Old World (progenitor) and putatively feral stocks were the most pesticide-tolerant. Furthermore, we found that activity of the detoxification enzyme esterase was positively correlated with pesticide tolerance when measured using two different substrate standards and confirmed that larvae from the Pol-Line stock had generally lower esterase activity. Consistent with an increased pesticide tolerance, the Old World and putatively feral stocks had higher esterase activities. However, esterases and other detoxification enzymes (CYP450s and GSTs) were found in similar abundances across stocks, suggesting that the differences in enzyme activity we observed might arise from stock-specific single nucleotide polymorphisms or post-translational modifications causing qualitative variation in enzyme activity. These results suggest that selective breeding may inadvertently increase honey bees’ sensitivity to pesticides, whereas unselected, putatively feral and Old World stocks have larvae that are more tolerant.