Caste‐ and pesticide‐specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees

Abstract

Social bees are important insect pollinators of wildflowers and agricultural crops, making their reported declines a global concern. A major factor implicated in these declines is the widespread use of neonicotinoid pesticides. Indeed, recent research has demonstrated that exposure to low doses of these neurotoxic pesticides impairs bee behaviours important for colony function and survival. However, our understanding of the molecular‐genetic pathways that lead to such effects is limited, as is our knowledge of how effects may differ between colony members. To understand what genes and pathways are affected by exposure of bumblebee workers and queens to neonicotinoid pesticides, we implemented a transcriptome‐wide gene expression study. We chronically exposed Bombus terrestris colonies to either clothianidin or imidacloprid at field‐realistic concentrations while controlling for factors including colony social environment and worker age. We reveal that genes involved in important biological processes including mitochondrial function are differentially expressed in response to neonicotinoid exposure. Additionally, clothianidin exposure had stronger effects on gene expression amplitude and alternative splicing than imidacloprid. Finally, exposure affected workers more strongly than queens. Our work demonstrates how RNA‐Seq transcriptome profiling can provide detailed novel insight on the mechanisms mediating pesticide toxicity to a key insect pollinator.

Thiamethoxam exposure deregulates short ORF gene expression in the honey bee and compromises immune response to bacteria

“…Glia are support cells of neurons and are protective in a number of ways. We noted that other studies found an overrepresentation of down-regulated genes with known function in immune and defence processes upon exposure to different types of neonicotinoids 18,26,67,68,75 . In contrast we did not find differentially regulated immune genes including the known AMPs in the brain.…”

“…Our study addresses the effect of thiamethoxam on gene expression at field relevant doses of thiamethoxam found in pollen and nectar. In particular we chose for these experiments a low and a high dose, which is about 0.04 ng and The sORFs we identified have not been reported in prior whole-transcriptome evaluations of neonicotinoid exposure in bee brains despite using similar concentrations of neonicotinoids 18,67,68 . A possible explanation for the different gene set we obtained after thiamethoxan exposure is that we analysed changes after long-term, low dose exposure, while prior studies used shorter exposures.…”

“…Changes in gene expression and processing of RNAs, including alternative splicing, are among the mechanisms available to an organism to adapt to environmental 4 perturbations 14,15 . Sub-lethal exposure to xenobiotics, such as pesticides, can alter alternative splicing [16][17][18] . Since many ion channel genes and other important neuronal genes undergo extensive alternative splicing, they are prime targets for changes induced by xenobiotics 17,19 .…”

Mating precedes selective immune priming which is maintained throughout bumblebee queen diapause

“…Scripts used for transcript quantification, differential expression and Gene Ontology enrichment analyses are modifications of the scripts published by Colgan et al [110]. The modified scripts used in the present study are archived at https://github.com/Joscolgan/bumblebee_proteomics.…”

Infection by the castrating parasitic nematode Sphaerularia bombi changes gene expression in Bombus terrestris bumblebee queens

“…The analysis of RNA-Seq libraries was performed using scripts modified from those made publicly available by Colgan et al (2019). Scripts for the present analysis are available at https:// github.com/Joscolgan/sphaerularia_rnaseq.…”