Sensory neuron population expansion enhances odor tracking without sensitizing projection neurons

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 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.

Comparative single-cell transcriptomic atlases reveal conserved and divergent features of drosophilid central brains

“…Moreover, the frequencies of the vast majority of presumed homologous cell types are conserved. This observation contrasts with studies of the peripheral olfactory system, where several olfactory sensory neuron population are increased (or decreased) in D. sechellia compared to the other species 32,33,38,40 . Our data provide empirical data to help answer the long-held question as to whether the sensory periphery is more evolvable than central brain regions 5 .…”

“…Our work provides an unprecedented comprehensive view of how animal brains evolve in a well-defined phylogenetic and ecological framework, by taking advantage of the relatively small brains of closely-related drosophilid species to generate and compare whole central brain cellular atlases. Previous studies on how the nervous system of D. sechellia differs from D. melanogaster and D. simulans have primarily focused on peripheral chemosensory pathways 28,[32][33][34][36][37][38]40 , leaving knowledge of potential adaptations in the brain almost completely unexplored. Despite the very different ecology and behaviors of the equatorial islandendemic specialist D. sechellia from its cosmopolitan, generalist relatives, the overall brain architecture of these flies is highly conserved.…”

“…For example, several populations of olfactory sensory neurons display increased sensitivity to noni-derived odors in D. sechellia compared to D. melanogaster and D. simulans, due to coding mutations in specific olfactory receptors. Furthermore, a number of olfactory sensory neuron populations are several-fold larger (or smaller) in D. sechellia, presumably due to changes in the developmental patterning of the olfactory organs 32,33,[38][39][40] .…”

Evolution of neural circuitry and cognition

“…Even where circuit motifs require multiple developmentally distinct cell types, motif number may be controlled through shared genetic regulation of motif components, or through selection to maintain co-evolutionary relationships of multiple cell type abundance. For example, across drosophilid species, circuit replication of olfactory sensory neurons is implicated in variation in sensory ecology while upstream projection and integrative neurons are highly conserved, but with specific morphological and physiological modifications [37,38,[68][69][70].…”

Changes in the cellular makeup of motor patterning circuits drive courtship song evolution inDrosophila

“…Where and how nervous systems have evolved to generate species diversity in complex motor behaviors remain largely unaddressed. Due to their rich behavioral differences and experimental accessibility, Drosophila species recently emerged as a promising system for species comparisons to explore the mechanisms by which behaviors evolve 3 , for example, linking species-specific host preferences and mate recognition to the evolution of sensory receptors and sensory circuits [4][5][6][7][8][9] .…”