Evolution of Two Receptors detecting the Same Pheromone Compound in Crop Pest Moths of the Genus Spodoptera

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

Shifts in sensory neuron identity parallel differences in pheromone preference in the European corn borer

Pheromone communication relies on highly specific signals sent and received between members of the same species. However, how pheromone specificity is determined in moth olfactory circuits remains unknown. Here we provide the first glimpse into the mechanism that generates this specificity in Ostrinia nubilalis. In Ostrinia nubilalis it was found that a single locus causes strain-specific, diametrically opposed preferences for a 2-component pheromone blend. Previously we found pheromone preference to be correlated with the strain and hybrid-specific relative antennal response to both pheromone components. This led to the current study, in which we detail the underlying mechanism of this differential response, through chemotopically mapping of the pheromone detection circuit in the antenna. We determined that both strains and their hybrids have swapped the neuronal identity of the pheromone-sensitive neurons co-housed within a single sensillum. Furthermore, neurons that mediate behavioral antagonism surprisingly co-express up to five pheromone receptors, mirroring the concordantly broad tuning to heterospecific pheromones. This appears as possible evolutionary adaptation that could prevent cross attraction to a range of heterospecific signals, while keeping the pheromone detection system to its simplest tripartite setup

A conserved odorant receptor detects the same 1-indanone analogs in a tortricid and a noctuid moth

Odorant receptors (ORs) interface animals with airborne chemical signals. They are under strong selection pressure and are therefore highly divergent in different taxa. Yet, some OR orthologs are highly conserved. These ORs may be tuned to odorants of broad importance, across species boundaries. Two widely distributed lepidopteran herbivores, codling moth Cydia pomonella (Tortricidae) feeding in apples and pears, and the African cotton leafworm Spodoptera littoralis (Noctuidae), a moth feeding on foliage of a wide range of herbaceous plants, both express a receptor ortholog, OR19, which shares 58% amino acid identity and 69% amino acid similarity. Following heterologous expression in the empty neuron system of Drosophila melanogaster, we show by single sensillum recordings that CpomOR19 and SlitOR19 show similar affinity to several substituted indanes. Tests with a series of compounds structurally related to 1-indanone show that 2-methyl-1-indanone, 2-ethyl-1-indanone, 3-methyl-1-indanone and 1-indanone elicit a strong response from both ORs. A keto group in position 1 is essential for biological activity and so are both rings of the indane skeleton. However, there is an important difference in steric complementary of the indane rings and the receptor. Methyl substituents on the benzene ring largely suppressed the response. On the other hand, alkyl substituents at position 2 and 3 of the five-membered ring increased the response indicating a higher complementarity with the receptor cavity, in both CpomOR19 and SlitOR19. Our results demonstrate a conserved function of an odorant receptor in two moths that are phylogenetically and ecologically distant. It is conceivable that a conserved OR is tuned to signals that are relevant for both species, although their ecological roles are yet unknown. Our finding demonstrates that functional characterization of ORs leads to the discovery of novel semiochemicals that have not yet been found through chemical analysis of odorants from insects and their associated host plants