De Novo Transcriptomic and Metabolomic Analyses Reveal the Ecological Adaptation of High-Altitude Bombus pyrosoma

SIMPLE SUMMARY: Bumblebees are very important pollinators for many wild and agricultural flowers and play significant roles in natural and agricultural ecosystems. The distribution of bumblebees varies between the species; some species occupy narrow areas, while others have a varied distribution from low to high elevation. Bombus pyrosoma is one of the bumblebee species with a highly varied geomorphological distribution range in China. To answer why some bumblebee species have a varied distribution, we compared the transcriptomic and metabolomic data of B. pyrosoma from the low-altitude North China Plain and the high-altitude Tibet Plateau. The results showed that energy metabolism and innate immunity of the high-altitude B. pyrosoma had been enhanced in order to adapt to the extreme environment of hypoxia and low temperature, compared to the low-altitude bumblebees. This study highlights the ecological adaptation of bumblebees distributed from low- to high-altitude conditions. ABSTRACT: Bombus pyrosoma is one of the most abundant bumblebee species in China, with a distribution range of very varied geomorphology and vegetation, which makes it an ideal pollinator species for research into high-altitude adaptation. Here, we sequenced and assembled transcriptomes of B. pyrosoma from the low-altitude North China Plain and the high-altitude Tibet Plateau. Subsequent comparative analysis of de novo transcriptomes from the high- and low-altitude groups identified 675 common upregulated genes (DEGs) in the high-altitude B. pyrosoma. These genes were enriched in metabolic pathways and corresponded to enzyme activities involved in energy metabolism. Furthermore, according to joint analysis with comparative metabolomics, we suggest that the metabolism of coenzyme A (CoA) and the metabolism and transport of energy resources contribute to the adaptation of high-altitude B. pyrosoma. Meanwhile, we found many common upregulated genes enriched in the Toll and immune deficiency (Imd)signaling pathways that act as important immune defenses in insects, and hypoxia and cold temperatures could induce the upregulation of immune genes in insects. Therefore, we suppose that the Toll and Imd signaling pathways also participated in the high-altitude adaptation of B. pyrosoma. Like other organisms, we suggest that the high-altitude adaptation of B. pyrosoma is controlled by diverse mechanisms.