Olfactory receptor and circuit evolution promote host specialisation

The evolution of animal behaviour is poorly understood(1,2). Despite numerous correlations of behavioural and nervous system divergence, demonstration of the genetic basis of interspecific behavioural differences remains rare(3–5). Here, we develop a novel neurogenetic model, Drosophila sechellia, a close cousin of D. melanogaster(6,7) that displays profound behavioural changes linked to its extreme specialisation on noni fruit(8–16). Using calcium imaging, we identify D. sechellia olfactory pathways detecting host volatiles. Mutational analysis indicates roles for different olfactory receptors in long- and short-range attraction to noni. Cross-species allele transfer demonstrates that tuning of one of these receptors is important for species-specific host-seeking. We identify the molecular determinants of this functional change, and characterise their evolutionary origin and behavioural significance. Through circuit tracing in the D. sechellia brain, we find that receptor adaptations are accompanied by increased sensory pooling onto interneurons and novel central projection patterns. This work reveals the accumulation of molecular, physiological and anatomical traits linked to behavioural divergence, and defines a powerful model for investigating nervous system evolution and speciation.