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

Abstract

Pheromone communication relies on highly specific signals sent and received between members of the same species. However, how pheromone preference is determined in moth olfactory circuits remains unknown. Here we describe a potential mechanism that generates preference differences 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 that pheromone preference was correlated with strain and hybrid-specific relative antennal response to both pheromone components. Here we detail the underlying mechanism of this differential response, through chemotopical mapping of the pheromone detection circuit in the antenna. We found 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. Co-expression appears evolutionarily advantageous as it prevents cross attraction to a range of heterospecific signals, while keeping the pheromone detection system to its simplest tripartite setup.