Integrative Analysis of Antennal Morphology and Olfactory Receptor Gene Expression Across the Three Castes of Bombus terrestris (Hymenoptera: Apidae)

TL;DR

This study explores how the sense of smell in bumblebee castes has evolved differently to suit their social roles and behaviors.

Contribution

The study reveals caste-specific adaptations in antennal structure and olfactory gene expression in Bombus terrestris.

Findings

Drones have longer sensilla and upregulated OR genes for queen pheromone detection.

Workers and queens show higher sensilla density and balanced gene expression for processing diverse signals.

Phylogenetic analysis suggests some OR genes originated from recent duplication events.

Abstract

This study investigates the adaptive differentiation of the olfactory system across Bombus terrestris castes through integrated morphological and transcriptomic analyses. Drones exhibit a “specialized” strategy characterized by elongated sensilla and upregulation of specific receptor genes for accurate queen pheromone detection, whereas workers and queens employ a “generalist” strategy featuring high sensilla density and balanced gene expression profiles to enable parallel processing of diverse chemical signals. These findings provide novel insights into the evolutionary mechanisms underlying chemical perception in social insects.

To systematically investigate how the olfactory system of Bombus terrestris adapts to its social division of labor and reproductive strategies, this study integrated the micromorphology of antennal sensilla and the expression profiles of olfactory receptor (OR) genes from the heads of its three castes (workers, drones, and queens) for a multi-level analysis. Scanning electron microscopy (SEM) revealed that drones possess significantly longer chaetic sensilla (Sch), sensilla trichodea (Str A/B), and sensilla basiconica (Sba A), as well as larger-diameter sensilla coeloconica (Sco) compared to workers and queens, indicating structural and functional specialization for sensitive detection of single key signals (e.g., queen pheromones). In contrast, workers and queens exhibited a more complete composition of sensilla types and a higher sensilla distribution density, suggesting the construction of a perceptual system capable of processing multiple chemical signals simultaneously. RNA-seq combined with qRT-PCR confirmed the significant upregulation of seven OR genes (e.g., BterOR3, BterOR4) in drones, while workers showed upregulation of BterOR3/5/7 accompanied by enrichment of P450 detoxification pathways. Phylogenetic analysis suggested that BterOR5 serves as a conserved co-receptor, and some OR genes may originate from recent duplication events. In summary, distinct differences were observed in the morphological structure and molecular expression of the olfactory system among B. terrestris castes. Drones exhibited structural and gene expression features consistent with specialization in queen pheromone detection, while workers and queens demonstrated sensilla diversity and olfactory receptor expression patterns indicative of a broader response capacity to diverse chemical signals. These findings support the view that the olfactory system has undergone multi-level adaptive evolution driven by social division of labor and reproductive roles.

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