Abstract
Sex pheromone receptors (PRs) are key players in chemical communication between mating partners in insects. In the highly diversified insect order Lepidoptera, male PRs tuned to female-emitted type I pheromones (which make up the vast majority of pheromones identified) form a dedicated subfamily of odorant receptors (ORs). Here, using a combination of heterologous expression and in vivo genome editing methods, we bring functional evidence that at least one moth PR does not belong to this subfamily but to a distantly related OR lineage. This PR, identified in the cotton leafworm Spodoptera littoralis, is highly expressed in male antennae and is specifically tuned to the major sex pheromone component emitted by females. Together with a comprehensive phylogenetic analysis of moth ORs, our functional data suggest two independent apparitions of PRs tuned to type I pheromones in Lepidoptera, opening up a new path for studying the evolution of moth pheromone communication.
Highlights
The use of pheromone signals for mate recognition is widespread in animals, and changes in sex pheromone communication are expected to play a major role in the rise of reproductive barriers and the emergence of new species (Smadja and Butlin, 2009)
SlitOr5 is highly expressed in males but does not belong to the type I pheromone receptor clade
Among the 20 paralogous lineages identified, SlitOR5 belonged to a lineage distantly related to the type I pheromone receptors (PRs) clade, as well as to the lineages containing type 0 and type II PRs (Figure 1B)
Summary
The use of pheromone signals for mate recognition is widespread in animals, and changes in sex pheromone communication are expected to play a major role in the rise of reproductive barriers and the emergence of new species (Smadja and Butlin, 2009). Previous studies suggested that moth pheromone receptors had appeared just once during evolution They revealed that these receptors belong to the same branch or lineage in the ‘family tree’ of all receptors that detect chemical compounds in moths. Bastin-Heline et al inserted this receptor into animal cells grown in the laboratory to confirm that it responds to a specific pheromone produced by S. littoralis They genetically modified moths of this species and showed that males need this receptor in order to mate. Based on a comprehensive phylogenetic analysis of lepidopteran ORs, we show that SlitOR5 belongs to an OR subfamily that is distantly related to the PR clade but harbors numerous sex-biased ORs from distinct moth families These results suggest that PRs detecting type I pheromones evolved at least twice in Lepidoptera, which offers a more detailed and complex panorama on moth PR evolution
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