Evolutionary Recoding of Olfactory Sensory Neurons

Odorant receptors ( Or s) are the interface between an animal’s nervous system and its olfactory environment. In insect genomes, the Or s 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 Or s. 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.