In Drosophila melanogaster the responses of many olfactory neurons to volatile chemicals are determined by the odorant receptor (Or) protein family. Or22a and Or22b are two tandemly arranged members that have resulted from a relatively young gene duplication. In the Canton-S laboratory strain both genes are present, but only Or22a is functional and determines the response of the ab3A class of olfactory neurons1. A copy number variant at this locus, Or22ab, is present at different frequencies in natural populations and at latitudinally varying frequency in Australia, suggesting the locus-specific action of selection2,3.
To investigate whether the Or22ab allele alters olfactory responses we generated individual isochromosomal lines from Australian natural populations and recorded responses from ab3A neurons. We found some lines had the same response profile as the Canton-S strain, and this correlated with two gene copies. However, in other lines we found a second phenotype with altered responses to many odorants, and this correlated with the Or22ab allele. Crucially, by expressing the Or22ab allele in empty neurons we showed that Or22ab mediates this phenotypic change in response profile. We further showed that behavioural responses to ecologically relevant odorants depend on whether Or22ab or Or22a is present, suggesting that changes to olfactory-driven behaviour may underly natural selection for the Or22ab allele.
We also identified a third naturally occurring ab3A phenotype, in which there are still two gene copies, but only Or22b is transcribed. We have thus identified at least three different molecular genetic changes at this locus that cause changes in the response profile of the ab3A neuron: (1) two genes are present and expressed but one encodes a non functional protein; (2) only one gene is present and expressed; and (3) two genes are present but only one is expressed.