Early hexapod genomes reveal the deep origin of insect gustatory and odorant receptors

Insect smell and taste is primarily mediated through a chemoreceptor superfamily that includes three lineages of gustatory receptors—sugar, carbon dioxide, and bitter—and a distinct lineage of odorant receptors. Although sugar gustatory receptors can be traced back to ancestral crustaceans, the evolutionary origins of the remaining lineages have been unclear. Here, we resolve this history through homology-driven searches and phylogenetic analyses across insect and non-insect hexapod genomes. We uncover several previously unrecognized gustatory receptor clades, including a fifth insect chemoreceptor lineage that we term relict gustatory receptors, which expanded in the non-insect hexapod order Diplura but dwindled in extant insects. We also identify a gustatory receptor lineage in non-insect hexapods that is sister to insect odorant receptors, and which provides strong evidence that odorant receptors arose from within the sugar gustatory receptors. These findings clarify relationships among the insect gustatory and odorant receptor lineages and illuminate the origins and subsequent diversification of chemoreception across Hexapoda. Insect smell and taste are governed by vast arrays of chemoreceptors, but the evolutionary origins of these genes have remained murky. This study resolves their origin through a phylogeny that incorporates numerous previously undescribed chemoreceptor lineages in insects and their near relatives.