Abstract
The Varroa destructor mite is a devastating parasite of Apis mellifera honeybees. They can cause colonies to collapse by spreading viruses and feeding on the fat reserves of adults and larvae. Amitraz is used to control mites due to its low toxicity to bees; however, the mechanism of bee resistance to amitraz remains unknown. In this study, we found that amitraz and its major metabolite potently activated all four mite octopamine receptors. Behavioral assays using Drosophila null mutants of octopamine receptors identified one receptor subtype Octβ2R as the sole target of amitraz in vivo. We found that thermogenetic activation of octβ2R-expressing neurons mimics amitraz poisoning symptoms in target pests. We next confirmed that the mite Octβ2R was more sensitive to amitraz and its metabolite than the bee Octβ2R in pharmacological assays and transgenic flies. Furthermore, replacement of three bee-specific residues with the counterparts in the mite receptor increased amitraz sensitivity of the bee Octβ2R, indicating that relative insensitivity of their receptor is the major mechanism for honeybees to resist amitraz. The present findings have important implications for resistance management and the design of safer insecticides that selectively target pests while maintaining low toxicity to non-target pollinators.
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All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all the figures.
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Funding
National Natural Science Foundation of China (31572039)
- Jia Huang
National Natural Science Foundation of China (32072496)
- Jia Huang
Zhejiang Provincial Outstanding Youth Science Foundation (LR19C140002)
- Jia Huang
National Institute on Deafness and Other Communication Disorders (DC007864)
- Craig Montell
National Institute on Deafness and Other Communication Disorders (DC016278)
- Craig Montell
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Huang et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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An octopamine receptor confers selective toxicity of amitraz on honeybees and Varroa mites
eLife 10:e68268.
https://doi.org/10.7554/eLife.68268
