Asymmetric Evolution of Antennal Cell Types Underlies a Derived Ammonia-Sensing Logic for Ecological Adaptation in...

Olfaction is crucial for insects adapting to agroecosystems and becoming significant crop pests, but how the antenna, a multicellular olfactory organ, is systematically organized at the cellular and molecular levels is not well understood. This study focuses on tephritids, particularly Bactrocera dorsalis, due to its global invasiveness and severe agricultural impact. We conducted comparative single-nucleus transcriptomics of the antennal olfactory organ in B. dorsalis and Drosophila melanogaster, revealing uneven transcriptomic divergence across cell types: structural cells showed higher cross-species similarity, while sensory neuronal populations and receptor expression were more divergent. Notably, in B. dorsalis, ammonia detection involves an additional candidate neuronal population with BdorAmt/BdorOrco transcript co-detection, contrasting with D. melanogaster, where ammonia detection is mediated by Amt-expressing neurons independently of Orco. This derived molecular sensing logic helps meet the ecological demands of B. dorsalis, in which females use ammonia as an important cue to locate bird droppings as a potential supplementary nutritional resource. Our results suggest that cell-type-dependent transcriptomic divergence may represent one important route through which insect olfactory systems adapt, with neuronal diversification contributing to molecular sensing pathways tailored to specific ecological demands.