Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid

Authors: LI, ZHIGUO - Fujian Agriculture And Forest University; YU, TIANTIAN - Fujian Agriculture And Forest University; Chen, Yanping - Judy; Heerman, Matthew; HE, JIANGFANG - Fujian Agriculture And Forest University; HUANG, JINGNAN - Fujian Agriculture And Forest University; NIE, HONGYI - Fujian Agriculture And Forest University; SU, SONGKUN - Fujian Agriculture And Forest University

Submitted to: Pesticide Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/3/2019
Publication Date: 2/4/2019
Citation: Li, Z., Yu, T., Chen, Y., Heerman, M.C., He, J., Huang, J., Nie, H., Su, S. 2019. Brain transcriptome of honey bees (Apis mellifera) exhibiting impaired olfactory learning induced by a sublethal dose of imidacloprid. Pesticide Biochemistry and Physiology. 156:36-43. https://doi.org/10.1016/j.pestbp.2019.02.001.
DOI: https://doi.org/10.1016/j.pestbp.2019.02.001

Interpretive Summary: There has been growing concern about the connection between bee population decline and the world's most widely-used class of insecticide --neonicotinoids. Imidacloprid is a neonicotinoid insecticide that has been reported to cause sense and smell learning deficits in honey bees via impairment of the target organ, the brain. We conducted a study to investigate the effects of Imidacloprid on honey bee learning capacity. Our results showed that brains of honey bees exposed to chronic oral imidacloprid treatmen for 11 days displayed a significantly higher level of oxidative stress and suppressed chemosensory responses compared to the negative control, which could possibly result in decreased olfactory learning capabilities in imidacloprid-treated bees. Our findings can contribute to a better understanding of the risks of neonicotinoid insecticides to honeybee performance and health. The results should be of interest to the researchers, graduate students, apiary inspectors, beekeepers and policymakers in the bee society worldwide.

Technical Abstract: Declines in honey bee populations represent a worldwide concern. The widespread use of neonicotinoid insecticides has been one of the factors linked to these declines. Sublethal doses of a neonicotinoid insecticide, imidacloprid, has been reported to cause olfactory learning deficits in honey bees via impairment of the target organ, the brain. In the present study, olfactory learning of honey bees was compared between controls and imidacloprid-treated bees. The brains of imidacloprid-treated and control bees were used for comparative transcriptome analysis by RNA-Seq to elucidate the effects of imidacloprid on honey bee learning capacity. The results showed that the learning performance of imidacloprid-treated bees was significantly impaired in comparison with control bees after chronic oral exposure to imidacloprid (0.02 ng/µl) for 11 days. Gene expression profiles between imidacloprid treatment and the control revealed that 131 genes were differentially expressed, of which 130 were downregulated in imidacloprid-treated bees. Validation of the RNA-Seq data using qRT-PCR showed that the results of qRT-PCR and RNA-Seq exhibited a high level of agreement. Gene ontology annotation indicated that the oxidation-reduction imbalance might exist in the brain of honey bees due to oxidative stress induced by imidacloprid exposure. KEGG and ingenuity pathway analysis revealed that transient receptor potential and Arrestin 2 in the phototransduction pathway were significantly downregulated in imidacloprid-treated bees, and that five downregulated genes have causal effects on behavioral response inhibition in imidacloprid-treated bees in imidacloprid-treated bees. Our results suggest that downregulation of brain genes involved in immune, detoxification and chemosensory responses may result in decreased olfactory learning capabilities in imidacloprid-treated bees.