Evolution of insect olfactory receptors

Christine Missbach,Marcus C Stensmyr,Ewald Grosse-Wilde,Bill S Hansson,Hany KM Dweck,Heiko Vogel,Andreas Vilcinskas

doi:10.7554/elife.02115

Christine Missbach, Marcus C Stensmyr + Show 5 more

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https://doi.org/10.7554/elife.02115

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Abstract

The olfactory sense detects a plethora of behaviorally relevant odor molecules; gene families involved in olfaction exhibit high diversity in different animal phyla. Insects detect volatile molecules using olfactory (OR) or ionotropic receptors (IR) and in some cases gustatory receptors (GRs). While IRs are expressed in olfactory organs across Protostomia, ORs have been hypothesized to be an adaptation to a terrestrial insect lifestyle. We investigated the olfactory system of the primary wingless bristletail Lepismachilis y-signata (Archaeognatha), the firebrat Thermobia domestica (Zygentoma) and the neopteran leaf insect Phyllium siccifolium (Phasmatodea). ORs and the olfactory coreceptor (Orco) are with very high probability lacking in Lepismachilis; in Thermobia we have identified three Orco candidates, and in Phyllium a fully developed OR/Orco-based system. We suggest that ORs did not arise as an adaptation to a terrestrial lifestyle, but evolved later in insect evolution, with Orco being present before the appearance of ORs. DOI: http://dx.doi.org/10.7554/eLife.02115.001.

Highlights

All living organisms, including bacteria, protozoans, fungi, plants, and animals, detect chemicals in their environment
To reconstruct an evolutionary scenario for insect olfactory receptors (ORs), we investigated species belonging to different ancient insect orders, including Archaeognatha and Zygentoma, and a neopteran insect belonging to the Phasmatodea as so far not analyzed control group using morphological, electrophysiological and molecular techniques
Our first step was to analyze the evolutionary ancestry of the insect olfactory system by assessing its complexity in each of three non-holometabolan insects

Summary

Introduction

All living organisms, including bacteria, protozoans, fungi, plants, and animals, detect chemicals in their environment. The sensitivity and chemical range of animal olfactory systems is remarkable, enabling animals to detect and discriminate between thousands of different odor molecules. There is a striking evolutionary convergence towards a conserved organization of signaling pathways in vertebrate and invertebrate olfactory systems (Hildebrand and Shepherd, 1997), the involved receptor gene families evolved independently. The molecular identity of olfactory receptors was first unraveled in vertebrates (Buck and Axel, 1991). As many as 1000 heterotrimeric GTP-binding protein (or G protein)-coupled receptors are considered to be employed in olfactory discrimination (Buck and Axel, 1991). A similar number of chemoreceptors, with about 1300 receptor genes and 400 pseudogenes, have been hypothesized for Caenorhabditis elegans (Robertson and Thomas, 2006)

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