Abstract
From 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 1-6 . 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 in Drosophila melanogaster and its close relative Drosophila sechellia , which feeds and breeds exclusively on Morinda citrifolia noni fruit 7-9 . We show that D. sechellia displays species-specific, large expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, and that this trait has a multigenic basis. In noni odour plume-tracking assays, D. sechellia exhibits enhanced performance compared to D. melanogaster . Through activation and inhibition of defined proportions of one noni-sensing OSN population, we establish that higher number of OSNs contributes to stronger, more persistent behaviour. OSN population expansions are accompanied by an increase in synaptic connections with their projection neuron (PN) partners that transmit information to higher brain centres. Quantification of odour-evoked activity of partner OSNs and PNs reveals that, surprisingly, larger numbers of OSNs does not lead to greater PN sensitivity or response reliability. Rather, these pathways - but not those with conserved OSN numbers - exhibit reduced adaptation of PN activity upon odour stimulation, likely through weakened lateral inhibition. 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.
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