Evolution of two receptors detecting the same pheromone compound in crop pest moths of the genus Spodoptera

Arthur De Fouchier,Olivier Mirabeau,Xiao Sun,Christelle Monsempes,Emmanuelle Jacquin-Joly,Nicolas Montagné

doi:10.3389/fevo.2015.00095

Abstract

In moths, mate finding strongly rely on the detection of sex pheromones by pheromone receptors. Any modification in the functional properties of these receptors can have a drastic impact on reproduction. In the course of characterizing candidate pheromone receptors in the noctuid moth Spodoptera littoralis, we expressed them in Drosophila olfactory sensory neurons and stimulated them with a large panel of moth pheromone compounds. We found that two pheromone receptors detect (Z,E)-9,12-14:OAc, a minor component of the female pheromone blend. Whereas SlitOR6 is highly specific to this component, SlitOR13 is less sensitive and not strictly specific as it also detects (Z)9-14:OAc, another minor component of the sex pheromone. Interestingly, SlitOR13 expression is restricted to the distal part of male antennae, where we could identify a novel functional class of pheromone-sensitive neurons whose response spectrum matches that of SlitOR13. Based on a phylogenetic analysis of Lepidoptera pheromone receptors, we built an evolutionary scenario in which four different paralogous lineages emerged through gene duplications. The ability to bind (Z,E)-9,12-14:OAc appeared independently within three of these lineages, and an analysis of selective pressures revealed sites under positive selection that could have played a role in the emergence of functional properties of OR6 and OR13 in Spodoptera species.

Highlights

In animals, various biological mechanisms prevent species from interbreeding with each other
Response Spectra of Heterologously Expressed SlitORs In order to systematically analyze the response spectra of SlitOR6, 11, 13 and 16 to a large panel of moth pheromone compounds, we expressed these receptors in Drosophila olfactory sensory neurons (OSNs) housed in at1 trichoid sensilla, in place of the endogenous pheromone receptors (PRs) DmelOR67d
The response spectrum of this OSN type matches that of SlitOR6, but no OSN detecting both (Z,E)-9,12-14:OAc and (Z)9-14:OAc, which would correspond to SlitOR13 response profile, was found. Considering that those electrophysiology studies focused on sensilla located on the proximal part of the antennae, where trichoid sensilla are abundant and easy to record, we investigated whether OSNs with a response profile matching that of SlitOR13 could be found on more distal parts of the antennae

Summary

Introduction

Various biological mechanisms prevent species from interbreeding with each other. One of the well-studied mechanisms of premating isolation is the sex pheromone communication system of moths (Cardé and Haynes, 2004). In those nocturnal insects, reproductive success largely depends on the long-distance detection of bouquets of air-borne chemicals usually emitted by the females. Most sex pheromones consist of a complex blend of a major component mixed with a few minor components, whose nature and precise relative ratios ensure a species-specific recognition (de Bruyne and Baker, 2008). Antennae bear thousands of sensilla housing olfactory sensory neurons (OSNs) that detect the different components of the pheromone blend with various. Numerous gene duplication events led to the variable number of putative PRs (usually from 4 to 9) found in the different species investigated (Krieger et al, 2004; Nakagawa et al, 2005; Wanner et al, 2010; Grosse-Wilde et al, 2011; Bengtsson et al, 2012; Zhang and Lofstedt, 2013; Steinwender et al, 2015)

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