Evolutionary Recoding of Olfactory Sensory Neurons

Abstract

Odorant receptors (Ors) are the interface between an animals nervous system and its olfactory environment. In insect genomes, the Ors are often the largest gene family, and their rapid duplications and deletions result in extensive copy-number differences between species. Because olfactory sensory neurons (OSNs) typically express only one Or (the so-called one-receptor one-neuron rule), this dynamism at the level of Or genes raises fundamental questions regarding their cellular regulation: How do new Or duplicates gain their own neuron-specific expression? Such Or-OSN changes are thought to provide a key evolutionary path for modifying olfactory perception and related behaviours, but the absence of examples of these transitions has prevented an understanding of how they occur. Using a highly duplicated Drosophila Or subfamily (the Or67a subfamily) as a model system, we discovered parallel instances of Or67a duplicates gaining new OSN expression and reconstructed their evolutionary histories. Functional work in D. suzukii, a species with two novel Or67a-expressing OSN populations, revealed that their Or67a expression has arisen in preexisting OSNs, which have lost their ancestral Ors. As a result, these neurons were recoded and acquired new olfactory identities, thereby demonstrating the diversification of an OSN repertoire without the invention of developmentally new OSN lineages.