Expression of Chemosensory Genes in Larval and Adult Cephalic Appendages in a Diving Beetle

The impact of land-to-water transition on chemosensory genes has been explored in marine tetrapod vertebrates, with scarce data on aquatic insect lineages. Diving beetles (Dytiscidae) are predaceous freshwater insects with strictly aquatic larvae and amphibious adults. Using RNA-seq, we compared the expression of odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), and odorant-binding proteins (OBPs) in the cephalic appendages of larval and adult Cybister lateralimarginalis. Overall, larvae expressed fewer chemosensory genes than adults but larva-specific genes displayed a unique expression pattern, not previously observed in any other holometabolous insect, with five larva-specific ORs all having a close paralogue which is adult-specific, 14 larva-specific IRs all belonging to a single gene expansion in the IR tree, and no larva-specific GR. Expression profiles across appendage types mirrored those in aerial insects, with ORs mainly in antennae, GRs in labial palps, "Antennal class" IRs in antennae, and "Divergent class" IRs in palps. This suggests that the land-to-freshwater transition in this lineage did not involve major changes in deployment of the major families of chemosensory genes among cephalic appendages. Notably, the expression of a substantial repertoire of ORs specifically in the antennae of the larva suggests that hydrophobic chemical cues are important for long-range chemodetection in freshwater, contrary to prevailing views about constraints for chemosensation within a water medium.