The origin of the odorant receptor gene family in insects

The sense of smell enables the detection and discrimination of airborne chemicals via chemosensory receptors that have evolved independently multiple times throughout the tree of life. In insects, the odorant receptor (OR) gene family is the major chemosensory gene family involved in olfaction and its origin has been hypothesized to coincide with the evolution of a terrestrial lifestyle in hexapods. Missbach et al. (2014) challenged this view and suggested that ORs evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality, hypothesizing that the OR/Orco system is an adaptation to winged flight in insects instead. Building upon this work, we investigated the genomes of basal hexapod and insect lineages including Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera in an effort to identify the origin of the insect OR gene family. While absent from all non-insect hexapod lineages analyzed, ORs are present in all insect genomes. Orco is absent only in the most ancient insect lineage Archaeognatha. A fully functional OR/Orco system was present in our newly generated genome data of the Zygentoma Thermobia domestica. We suggest that ORs did evolve as adaptation to a terrestrial lifestyle outside high-humidity habitats, and not winged flight, representing a key evolutionary novelty in the ancestor of all insects. The OR family is therefore the first known molecular synapomorphy for the Class Insecta.