The origin of the odorant receptor gene family in insects

Abstract

The origin of the insect odorant receptor (OR) gene family has been hypothesized to have coincided with the evolution of terrestriality in insects. Missbach et al. (2014) suggested that ORs instead evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality and the OR/Orco system is an adaptation to winged flight in insects. We investigated genomes of the Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera, and find ORs present in all insect genomes but absent from lineages predating the evolution of insects. Orco is absent only in the ancestrally wingless insect lineage Archaeognatha. Our new genome sequence of the zygentoman firebrat Thermobia domestica reveals a full OR/Orco system. We conclude that ORs evolved before winged flight, perhaps as an adaptation to terrestriality, representing a key evolutionary novelty in the ancestor of all insects, and hence a molecular synapomorphy for the Class Insecta.

The genome of the blind soil-dwelling and ancestrally wingless dipluranCampodea augens, a key reference hexapod for studying the emergence of insect innovations

“…However, studies of the genomic chemosensory amenities of Diplura are scarce. Brand et al (2018) noted that the sequenced genome of the dipluran C. aquilonaris contains no odorant receptor (OR) gene family members. We likewise were unable to identify ORs or the Odorant receptor co-receptor (Orco) in the C. augens genome.…”

“…This analysis excludes the few available partial GR sequences from two orders of early diverging insects (Archaeognatha and Zygentoma) (Missbach et al 2014). Unfortunately, the available draft genomes of these two orders are too fragmented to reliably annotate their GRs (Brand et al 2018), and the GRs have been only partially annotated for one of the three draft genomes of Collembola (Wu et al 2017). Given the phylogenetic distance of Diplura to Collembola and ancestrally wingless insects (i.e., Archaeognatha and Zygentoma), inclusion of their GRs is unlikely to change our assessment of the dipluran GR complement.…”

Genomic adaptations to aquatic and aerial life in mayflies and the origin of wings in insects

“…Since temporal gene expression profiling indicated a prominent role of genes involved in perception of chemical cues during C. dipterum aquatic phase, we investigated in its genome the five main chemosensory (CS) gene families in arthropods. These include the odorant receptor/odorant receptor cofactor (OR/ORCO) and the odorant binding protein family (OBP), both of which have been suggested to play essential roles during the evolution of terrestrialization in hexapods and insects [21][22][23][24][25][26][27] .…”

Mushroom Body Homology and Divergence across Pancrustacea

“…Thus, up to the lateral protocerebrum, each level of the olfactory pathway typifies either a crustacean or an insect (Table 2). No crustacean possesses ligand-gated ORNs, and hexapod molecular phylogenetics implies that the insect odorant receptor family (ORs; Brand et al, 2018) appeared after terrestrialization (Missbach et al, 2014). In crustaceans, arrangements amongst ORN terminals and widely branching PNs implies all-to-all connectivity.…”