Evolutionary Dynamics of the Complete Chemosensory Repertoire in Kissing Bugs of the Genus Rhodnius: Divergent Odorant Receptors Contrast with Conserved Gene Families

Abstract

Chemosensory systems play a central role in host detection, feeding behavior, and habitat selection in hematophagous insects. Here, we performed a comparative evolutionary analysis of chemosensory gene repertoires across 13 species of the Chagas disease vector genus Rhodnius. While gustatory receptors (GRs), ionotropic receptors (IRs), odorant-binding proteins (OBPs), and chemosensory proteins (CSPs) remained globally conserved, odorant receptors (ORs) displayed extensive lineage-specific expansions, tandem duplications, dynamic transcriptomic regulation, and recurrent signatures of positive selection. Major OR expansions were observed in Rhodnius robustus and Rhodnius colombiensis, suggesting increased sensory diversification in ecologically heterogeneous lineages. In contrast, conserved GR1 expression supports the maintenance of ancestral sugar-detection pathways despite hematophagy lifestyle. We further found no evidence of the canonical insect CO2-associated GRs, suggesting alternative molecular mechanisms for CO2 perception in Triatominae. Several receptors, including Orco, also displayed shifts in selective constraints between sylvatic and domiciliary species, consistent with sensory remodeling associated with adaptation to domestic habitats. Together, our results identify ORs as the most evolutionarily dynamic component of the Rhodnius chemosensory repertoire and highlight contrasting evolutionary trajectories among chemosensory gene families during ecological diversification and vector adaptation.