Smelling in the dark: Phylogenomic insights into the chemosensory system of a subterranean beetle

The chemosensory system has experienced relevant changes in subterranean animals, facilitating the perception of specific chemical signals critical to survival in their particular environment. However, the genomic basis of chemoreception in cave-dwelling fauna has been largely unexplored. We generated de novo transcriptomes for antennae and body samples of the troglobitic beetle Speonomus longicornis (whose characters suggest an extreme adaptation to a deep subterranean environment) in order to investigate the evolutionary origin and diversification of the chemosensory gene repertoire across coleopterans through a phylogenomic approach. Our results suggested a diminished diversity of odourant and gustatory gene repertoires compared to polyphagous beetles that inhabit surface habitats. Moreover, S. longicornis showed a large diversity of odourant-binding proteins, suggesting an important role of these proteins in capturing airborne chemical cues. We identified a gene duplication of the ionotropic coreceptor IR25a, a highly conserved single-copy gene in protostomes involved in thermal and humidity sensing. In addition, no homologous genes to sugar receptors or the ionotropic receptor IR41a were detected. Our findings suggest that the chemosensory gene repertoire of this cave beetle may result from adaptation to the highly specific ecological niche it occupies, and that gene duplication and loss may have played an important role in the evolution of gene families involved in chemoreception. Altogether, our results shed light on the genomic basis of chemoreception in a cave-dwelling invertebrate and pave the road towards understanding the genomic underpinnings of adaptation to the subterranean lifestyle at a deeper level.This work was supported by the Ministerio de Economía y Competitividad and the Ministerio de Ciencia of Spain (CGL2016-76705-P to Ignacio Ribera, PID2019-108824GA-I00 to Rosa Fernández, and CGL2016-75255 and PID2019-103947GB to Julio Rozas). Pau Balart-García and Paula Escuer were supported by an FPI grant (Ministerio de Economía y Competitividad BES-2017-081050 and BES-2017-081740, respectively). Rosa Fernández was supported by a Marie Sklodowska-Curie grant (747607) and a Ramón y Cajal fellowship (Ministerio de Economía y Competitividad, RyC2017-22492).Peer reviewe