Evolution of Acid-Sensing Olfactory Circuits in Drosophilids

Animals adapt their behaviors to specific ecological niches, but the genetic and cellular basis of nervous system evolution is poorly understood. We have compared the olfactory circuits of the specialist Drosophila sechellia—which feeds exclusively on Morinda citrifolia fruit—with its generalist cousins D. melanogaster and D. simulans. We show that D. sechellia exhibits derived odor-evoked attraction and physiological sensitivity to the abundant Morinda volatile hexanoic acid and characterize how the responsible sensory receptor (the variant ionotropic glutamate receptor IR75b) and attraction-mediating circuit have evolved. A single amino acid change in IR75b is sufficient to recode it as a hexanoic acid detector. Expanded representation of this sensory pathway in the brain relies on additional changes in the IR75b promoter and trans-acting loci. By contrast, higher-order circuit adaptations are not apparent, suggesting conserved central processing. Our work links olfactory ecology to structural and regulatory genetic changes influencing nervous system anatomy and function. •D. sechellia, but not D. melanogaster, is attracted by hexanoic acid, a key host odor•D. sechellia IR75b evolved hexanoic acid sensitivity through a single residue change•Cis- and trans-acting mutations expanded the IR75b neuron population in D. sechellia•Conserved central circuits downstream of IR75b mediate attraction in D. melanogaster Prieto-Godino et al. characterize the genetic basis of the evolution of acid-sensing olfactory circuits in drosophilids, identifying structural and regulatory mutations that determine physiological and neuroanatomical differences between ecologically-distinct species.