Evolution of insect olfactory receptors

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

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

“…To confirm that these behavioural effects impact flight behaviour, our wind-tunnel results show that disruption of intracellular signalling in OR-expressing cells reduces the ability of flies to track odours from long distances and also reduces the success of odour localization. This line of experimentation supports the hypothesis that the evolution of the OrX-Orco complex in flying insects (Missbach et al, 2014) may have occurred to accommodate the high-speed demands of odourmediated tracking while in flight (Getahun et al, 2012). Obviously, a similar role for intracellular signalling in ORs of other pterygote orders must be demonstrated to give credence to this hypothesis.…”

“…Silbering and Benton (2010) also note that the independent evolution of two different chemosensory ion channel families in insects 'argues against the emergence of the observed dichotomy by "chance", and rather points towards specific mechanistic advantages'. Missbach et al (2014) also suggest that olfactory receptors evolved at the same point in time that vascular plants spread and insects evolved flight. This line of evidence raises a hypothesis that the evolution of the unique heteromeric OR complex found in pterygotes might have conferred a specific mechanistic advantage to insects during flight.…”

“…While IRs are common to all protostomes (Croset et al, 2010), a recent study by Missbach et al (2014) indicates the heterodimer OR complex is unique to pterygote insect orders. The co-receptor Orco is highly conserved in insects and Orco homologues have been identified in moths, flies, beetles, social insects and true bugs (Missbach et al, 2014;Krieger et al, 2003;Pitts et al, 2004;Smadja et al, 2009;Yang et al, 2012). Silbering and Benton (2010) also note that the independent evolution of two different chemosensory ion channel families in insects 'argues against the emergence of the observed dichotomy by "chance", and rather points towards specific mechanistic advantages'.…”

Comparing the Expression of Olfaction-Related Genes in Gypsy Moth (Lymantria dispar) Adult Females and Larvae from One Flightless and Two Flight-Capable Populations

“…Recent reports suggest there are multiple variant IRs with different ligand-binding domains that lack the characteristic glutamate-interacting residues (Benton et al, 2009). Unlike ORs, which are exclusively found in pterygote insects, IRs are present in all protostome species studied so far and may have evolved as long as 550-850 million years ago (Croset et al, 2010;Missbach et al, 2014). Similar iGluR-like genes are also present in plants, animals and prokaryotes, indicating that this is an important and ancient group of chemoreceptors (Benton et al, 2009;Rytz et al, 2013).…”

“…Since host-plant location and oviposition in herbivorous insects are largely mediated by chemical cues (Bruce et al, 2005;Bruce and Pickett, 2011;Mescher and De Moraes, 2015), one would expect the evolution of flight to be accompanied by the development of sophisticated olfactory systems. New evidence even suggests that the odorant receptor family (OR), central to the olfactory systems of highly derived insects, emerged around the same time as flight (Missbach et al, 2014;Ioannidis et al, 2017). Furthermore, manipulation of OR-based odor detection in Drosophila also indicates that ORs play an important role in flight orientation (Getahun et al, 2016).…”