Evolutionary dynamics of insect odorant receptors reveal ecological tuning shaping olfactory perception

Insect olfaction is facilitated by a heterotetrameric odorant receptor-odorant receptor co-receptor (OR-Orco) complex, which is distinct from that of vertebrate ORs. However, extreme sequence divergence among insect ORs has hindered a unified understanding of their evolutionary history and ecological importance. In this study, we present a multiscale analysis of OR genes across 115 insect species. We overcome the limitations of traditional phylogenetic approaches by applying a protein similarity network-based strategy and introduce a "trunk-branch" framework to systematically describe the evolutionary trajectories of insect ORs across sequence, structural, and functional levels. Although they possess different sequences and structural communities, all the insect orders were found to contain fully functional OR repertoires. Notably, insects adapted to end-Permian mass extinction through shifts in their functional OR repertoires, and early- and late-diverging lineages exhibit distinct patterns of OR differentiation. The emergence of Orco represents a key evolutionary transition point, marking the shift from a homomeric to a heteromeric complex accompanied by specialization of the extracellular domain and binding pocket. Furthermore, we established robust associations between olfactory recognition breadth and ecological variables, including diet, circadian rhythm, and habitat. Our findings provide a comprehensive framework for the evolution of insect ORs, explaining the complex adaptive relationship between insect olfactory potential and diverse ecological environments.