The origin of the odorant receptor gene family in insects.

Philipp Brand,Brian R Johnson,Hugh M Robertson,Juan Luis Jurat-Fuentes,William E Klingeman,Wei Lin,Ratnasri Pothula

doi:10.7554/elife.38340

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.

Highlights

From bacteria to mammals, living organisms of all levels of complexity have evolved chemosensory receptors to detect and discriminate chemicals in the environment (Wuichet and Zhulin, 2010; Hansson and Stensmyr, 2011)
In an effort to identify the origin of the insect odorant receptor (OR) gene family and the OR co-receptor (Orco)/OR system, we investigated the genome sequences of species belonging to multiple insect and other terrestrial hexapod orders (Figure 1), Collembola, Diplura, Figure 1
We detected no ORs in two non-insect hexapod lineages, Collembola and Diplura, despite extensive annotation efforts

Summary

Introduction

From bacteria to mammals, living organisms of all levels of complexity have evolved chemosensory receptors to detect and discriminate chemicals in the environment (Wuichet and Zhulin, 2010; Hansson and Stensmyr, 2011). Given evidence that IRs serve olfactory roles in terrestrial crustaceans and insects (Rytz et al, 2013; Groh-Lunow et al, 2014; Rimal and Lee, 2018), they argued that olfaction in terrestrial noninsect hexapods and apterygote insects is entirely IR-dependent, with Orco evolving as ancestral OR from the GR lineage between the Archaeognatha and Zygentoma Based on these findings, Missbach et al (2014) suggested that the Orco/OR system evolved together with flight in pterygote insects and left off with the observation that ‘the existence of three Orco types remains mysterious’. Archaeognatha (jumping bristletails), Zygentoma (silverfish and firebrats), Odonata (damselflies and dragonflies), and Ephemeroptera (mayflies)

Results and discussion

Materials and methods

Funding Funder National Science Foundation