Comparative Genomics of the Major Chemosensory Gene Families in Arthropods

Abstract

Abstract Chemoreception is the most important sense for the survival and reproduction of most animal species. In insects, the principal proteins involved in the recognition of chemical cues comprise moderately sized, multigene families. These families include (i) odorant‐binding (OBPs) and chemosensory (CSPs) proteins, which are involved in peripheral olfactory processing; (ii) the chemoreceptor super‐family, formed by the olfactory (OR) and gustatory (GR) receptors; and (iii) the ionotropic receptors (IR), a variant class of ionotropic glutamate receptors (iGluR). Recent comparative genomic analyses of fully sequenced arthropod genomes support the birth‐and‐death model as the major evolutionary mechanism in determining the chemosensory repertoire size, and provide evidence of adaptive changes fostered by ecological shifts that might influence the current size of chemosensory families. These studies also advocate for the origin of olfactory gene families with the evolution of terrestriality in insects. Key Concepts: The chemosensory system mediates the detection of food, predators and mates, eliciting feeding behaviours and innate sexual and reproductive responses. In arthropods, the most important proteins involved in the recognition of chemical cues comprise moderately sized multigene families. The chemosensory system of arthropods relies on transmembrane receptors (OR, GR and IR gene families) and small globular proteins (OBP and CSP families). The number of chemosensory genes is similar across the Drosophila genus, with little variation in the gene number among species. New OBP and CSP genes appear by gene duplication in extant chromosomal clusters, and diverge independently from each other. An unexpectedly high number of gene gains and losses occurred in the evolution of chemosensory families during the 40–60 Myr of divergence of the Drosophila genus. The chemosensory families in insects evolve under a birth‐and‐death process, with lineage‐specific family size expansions and contractions at large time scale. The selective constraints on chemosensory genes have varied over the evolution of the Drosophila genus, with some cases of positive selection. Random genomic drift, assisted by eventual adaptation processes, is the principal determinant of the chemosensory family size of arthropods.