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. 2023 Mar;32(5):1034-1044.
doi: 10.1111/mec.16811. Epub 2023 Jan 17.

Expression of subunits of an insecticide target receptor varies across tissues, life stages, castes, and species of social bees

Alicja Witwicka  1 , Federico López-Osorio  1 , Valentine Patterson  1 , Yannick Wurm  1   2   3
Affiliations

Expression of subunits of an insecticide target receptor varies across tissues, life stages, castes, and species of social bees

Alicja Witwicka et al. Mol Ecol. 2023 Mar.

Abstract

Global losses of insects jeopardize ecosystem stability and crop pollination. Robust evidence indicates that insecticides have contributed to these losses. Notably, insecticides targeting nicotinic acetylcholine receptors (nAChRs) have neurotoxic effects on beneficial insects. Because each nAChR consists of five subunits, the alternative arrangements of subunits could create a multitude of receptors differing in structure and function. Therefore, understanding whether the use of subunits varies is essential for evaluating and predicting the effects of insecticides targeting such receptors. To better understand how the use and composition of nAChRs differ within and between insect pollinators, we analysed RNA-seq gene expression data from tissues and castes of Apis mellifera honey bees and life stages and castes of the Bombus terrestris bumble bees. We reveal that all analysed tissues express nAChRs and that relative expression levels of nAChR subunits vary widely across almost all comparisons. Our work thus shows fine-tuned spatial and temporal expression of nAChRs. Given that coexpression of subunits underpins the compositional diversity of functional receptors and that the affinities of insecticides depend on nAChR composition, our findings provide a likely mechanism for the various damaging effects of nAChR-targeting insecticides on insects. Furthermore, our results indicate that the appraisal of insecticide risks should carefully consider variation in molecular targets.

Keywords: Apis mellifera; Bombus terrestris; bees; gene expression; neonicotinoid pesticides; nicotinic acetylcholine receptors; pollinator health.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

FIGURE 1
FIGURE 1
The expression of nAChR subunits differs between tissues and between castes. (a) Honey bee tissues we analysed in gene expression comparisons of nAChR subunits. (b–c) Total combined expression of nAChR subunits in honey bee (Apis mellifera) queen brain and nine tissues of workers (b), bumble bee (Bombus terrestris) queen and worker heads, and whole bodies of worker adults, larvae, and pupae (c). The bar charts show the mean of the counts and the standard deviation. Values in b and c were normalized across samples and studies using DESeq2. (d) Topological representation of the phylogeny of nAChR subunits (Jones et al., 2006); dashed line to subunit α9 indicates that the bumble bee lacks this subunit. (e–f) The ratio of expression of nAChR subunits varies in honey bees (e; 11 genes) and bumble bees (f; 10 genes) (Wald tests, FDR < 0.05). The parentheses show the number of biological replicates for each sample type.
FIGURE 2
FIGURE 2
Source of and relationships among samples. (a) Datasets we analyzed in each comparison. We detected differences in the baseline levels of nAChR subunit expression using samples of untreated bees. In analyses combining data from independent studies, we used the RUVSeq method to correct potential batch effects caused due to technical differences (see Materials and Methods). (b–d) Principal component analyses show relationships among samples of (b) nine tissues of A. mellifera workers, (c) brains of queens and workers of A. mellifera corrected for the study batch effect, and (d) developmental stages of B. terrestris.
FIGURE 3
FIGURE 3
The expression levels (VST counts) of nAChR subunits in all Apis mellifera samples. (a) Count data of samples included in the analysis of honey bee tissues. (b) Count data of samples used in the analysis comparing brains of queens and workers, gathered from multiple sources. Removing batch effects from the transformed counts allows comparing the amounts of nAChRs subunits between castes and across source studies.
FIGURE 4
FIGURE 4
Differences in nAChR subunit expression between species. Interspecies comparisons excluded the divergent subunits α9 and β2 and relied solely on the single‐copy orthologous subunits. Pairwise comparisons of median subunit proportions revealed high positive correlations (Spearman's coefficients) between independent studies of each caste per species; numbers indicate Spearman's ρ values (a). The use of nAChR subunits differs between honey bees and bumble bees in the brains of queens (b) (Spearman's ρ = 0.52, p = 0.16) and workers (c) (Spearman's ρ = 0.30, p = 0.44); we fitted the regression lines using the least squares method.
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