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While many studies have examined the effects of neonicotinoid insecticides and the parasitic mite  Varroa destructor  on honey bees ( Apis mellifera ), more information on the combined effects of such stressors on gene expression, including neural related genes, and their impact on biological pathways is needed. This study analyzed the effects of field realistic concentrations of the neonicotinoid clothianidin on adult bees infested and not infested with  V .  destructor  over 21 consecutive days and then determined bee survivorship, weight, deformed wing virus (DWV) levels and gene expression.  V .  destructor  parasitism with or without clothianidin exposure was significantly associated with decreased survivorship, weight loss and higher DWV levels, while clothianidin exposure was only associated with higher levels of DWV. Expression analysis of the neural genes  AmNlg-1 ,  BlCh  and  AmAChE-2  showed that  V .  destructor  caused a significant down-regulation of all of them, whereas clothianidin caused a significant down-regulation of only  AmNrx-1  and  BlCh . An interaction was only detected for  AmNrx-1  expression. RNAseq analysis showed that clothianidin exposure resulted in 6.5 times more up-regulated differentially expressed genes (DEGs) than  V .  destructor  alone and 123 times more than clothianidin combined with  V .  destructor . Similar results were obtained with down-regulated DEGs, except for a higher number of DEGs shared between  V .  destructor  and the combined stressors. KEGG (Kyoto Encyclopedia of Genes and Genomes) biological pathway analysis of the DEGs showed that the stressor linked to the highest number of KEGG pathways was clothianidin, followed by  V .  destructor , and then considerably fewer number of KEGG pathways with the combined stressors. The reduced numbers of DEGs and KEGG pathways associated with the DEGs for the combined stressors compared to the stressors alone indicates that the interaction of the stressors is not additive or synergistic, but antagonistic. The possible implications of the antagonistic effect on the number of DEGs are discussed.

plos one

Interaction of field realistic doses of clothianidin and Varroa destructor parasitism on adult honey bee (Apis mellifera L.) health and neural gene expression, and antagonistic effects on differentially expressed genes