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Description
The suborder Adephaga, second suborder of Coleoptera in species number, includes families from a wide range of ecological environments, from terrestrial to aquatic. Multiple independent transitions from land to water within this group provide a valuable model for studying how the olfactory system adapted to different environments. Given the distinct properties of chemical diffusion in air versus water, chemosensory evolution is expected to reflect major morphological and molecular shifts. Our work investigates the evolution of the chemosensory system in aquatic Adephagan-beetles, using a transcriptomic approach. First, a total of 24 transcriptomes were sequenced, assembled, annotated, and their expression were quantified among antennae and palps from species representing seven Adephagan families, including both terrestrial and aquatic species. Secondly, a case study on Cybister lateralimarginalis (Dytiscidae) involved comparing gene expression across different cephalic organs in both larval and adult stages.
Taken together, our results show that in terrestrial Adephaga, odorant receptors (ORs) are predominantly expressed in the antennae, with no evidence of ORs exclusively expressed in the maxillary palps. In contrast, aquatic species exhibit clades of ORs specifically expressed in the maxillary palps. Notably, two of these clades show substantial gene duplications (expansions) that are specific to aquatic families. We hypothesize that these maxillary-palp-specific ORs are localized to a lateral olfactory field on the palp, as supported by scanning electron microscopy (SEM) and in situ hybridization targeting the co-receptor Orco. In Dytiscidae larva, we also identified a set of larval-specific ORs that are not expressed in adult, suggesting stage-specific olfactory functions and further diversification of the chemosensory system across developmental stages. These results highlight a striking divergence in the olfactory system between terrestrial and aquatic Adephaga, with evidence for molecular innovations pointing to a major evolutionary shift in chemosensory strategies associated with habitat transition.
