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

PLoS One. 2020 Feb 20;15(2):e0229030. doi: 10.1371/journal.pone.0229030. eCollection 2020.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bees / drug effects*
  • Bees / genetics*
  • Bees / parasitology*
  • Computational Biology
  • Gene Expression Profiling
  • Gene Expression Regulation / drug effects*
  • Guanidines / pharmacology*
  • Host-Parasite Interactions / drug effects*
  • Host-Parasite Interactions / genetics*
  • Insecticides / pharmacology*
  • Kaplan-Meier Estimate
  • Neonicotinoids / pharmacology*
  • Thiazoles / pharmacology*

Substances

  • Guanidines
  • Insecticides
  • Neonicotinoids
  • Thiazoles
  • clothianidin

Associated data

  • Dryad/10.5061/dryad.9w0vt4bbg

Grants and funding

The Project was funded in part by the Agricultural Research Institute of Ontario, the Ontario Ministry of Agriculture, Food and Rural Affairs, and by a grant from the Pinchin family to EG. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.