Sensory neuron population expansion enhances odour tracking through relaxed projection neuron adaptation

Abstract

AbstractFrom the star-nosed mole’s eponymous mechanosensory organ to the platypus’ electroreceptive bill, the expansion of sensory neuron populations detecting important environmental cues is a widespread evolutionary phenomenon in animals1–6. How such neuron increases contribute to improved sensory detection and behaviour remain largely unexplained. Here we address this question through comparative analysis of olfactory pathways inDrosophila melanogasterand its close relativeDrosophila sechellia, which feeds and breeds exclusively onMorinda citrifolianoni fruit7–9. We show thatD. sechelliadisplays selective, large expansions of noni-detecting olfactory sensory neuron (OSN) populations, and that this trait has a multigenic basis. These expansions are accompanied by an increase in synaptic connections between OSNs and their projection neuron (PN) partners that transmit information to higher brain centres. Quantification of odour-evoked responses of partner OSNs and PNs reveals that OSN population expansions do not lead to heightened PN sensitivity, beyond that due to sensory receptor tuning differences. Rather, these pathways – but not those with conserved OSN numbers – exhibit non-adapting PN activity upon odour stimulation. In noni odour plume-tracking assays,D. sechelliaexhibits enhanced performance compared toD. melanogaster. Through activation and inhibition of defined proportions of a noni-sensing OSN population, we establish that increased neuron numbers contribute to this behavioural persistence. Our work reveals an unexpected functional impact of sensory neuron expansions that can synergise with peripheral receptor tuning changes to explain ecologically-relevant, species-specific behaviour.