Functional and molecular evolution of olfactory neurons and receptors for aliphatic esters across the Drosophila genus
Insect olfactory receptor (Or) genes are large, rapidly evolving gene families of considerable interest for evolutionary studies. They determine the responses of sensory neurons which mediate critical behaviours and ecological adaptations. We investigated the evolution across the genus Drosophila of a subfamily of Or genes largely responsible for the perception of ecologically relevant aliphatic esters; products of yeast fermentation and fruits. Odour responses were recorded from eight classes of olfactory receptor neurons known to express this Or subfamily in D. melanogaster and from homologous sensilla in seven other species. Despite the fact that these species have diverged over an estimated 40 million years, we find that odour specificity is largely maintained in seven of the eight species. In contrast, we observe extensive changes in most neurons of the outgroup species D. virilis, and in two neurons across the entire genus. Some neurons show small shifts in specificity, whilst some dramatic changes correlate with gene duplication or loss. An olfactory receptor neuron response similarity tree did not match an Or sequence similarity tree, but by aligning Or proteins of likely functional equivalence we identify residues that may be relevant for odour specificity. This will inform future structure–function studies of Drosophila Ors.
KeywordsOlfaction Evolution Odour response profile Receptor neurons Olfactory receptors
Olfactory receptor neuron
Polymerase chain reaction
We thank Rebecca Hallas (Ary Hoffmann lab) and Rob Good (Charles Robin lab) from the University of Melbourne for D. ananassae and D. serrata stocks. We also thank Jyotika Taneja (Monash University) for maintaining fly stocks and Stephen Trowell (CSIRO Entomology, Canberra) for comments on the manuscript. We thank two anonymous reviewers for their helpful suggestions for improvements to the manuscript. This work was funded by a grant from the Collaboration fund of CSIRO’s Food Futures Flagship, Australia. All experiments comply with “principles of animal care”, publication No. 86-23, revised 1985 of the National Institute of Health, and also with the current laws of Australia
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