Olfactory sensory neuron population expansions influence projection neuron adaptation and enhance odour tracking
The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous olfactory pathways of Drosophila melanogaster and its close relative Drosophila sechellia, an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN number increases contribute to stronger, more persistent, noni-odour tracking behaviour. These expansions result in increased synaptic connections of sensory neurons with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odour-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron population expansions to explain ecologically-relevant, species-specific behaviour.
Authors
- Lucia L. Prieto-Godino (ORCID: https://orcid.org/0000-0002-2980-362X)
- Thomas O. Auer (ORCID: https://orcid.org/0000-0003-3442-0567)
- Floris van Breugel (ORCID: https://orcid.org/0000-0001-6538-7179)
- Steeve Cruchet (ORCID: https://orcid.org/0000-0001-7796-6151)
- Carl F. R. Wienecke (ORCID: https://orcid.org/0000-0003-3022-0218)
- Liliane Abuin
- Gizem Sancer (ORCID: https://orcid.org/0000-0002-0367-9421)
- Raquel Álvarez-Ocaña (ORCID: https://orcid.org/0009-0000-5135-4173)
- S. Takagi (ORCID: https://orcid.org/0000-0002-6381-7152)
- David L. Stern (ORCID: https://orcid.org/0000-0002-1847-6483)
- Richard Benton (ORCID: https://orcid.org/0000-0003-4305-8301)
- James M. Jeanne (ORCID: https://orcid.org/0000-0001-7657-202X)
- S. David Stupski (ORCID: https://orcid.org/0000-0001-5158-9386)
- J. Roman Arguello (ORCID: https://orcid.org/0000-0001-7353-6023)
Institutions
- University of Nevada, Reno (US)
- Howard Hughes Medical Institute (US)
- Harvard University (US)
- University of Fribourg (CH)
- Queen Mary University of London (GB)
- Janelia Research Campus (US)
- The Francis Crick Institute (GB)
- Yale University (US)
- Stanford University (US)
- University of Lausanne (CH)
Publication Details
- Journal
- Nature Communications
- Published
- 2024-08-15
- DOI
- https://doi.org/10.1038/s41467-024-50808-w
- Citations
- 20
- Primary Topic
- Olfactory and Sensory Function Studies
- Type
- article
- Field-Weighted Citation Impact
- 7.22
Funders
- National Science Foundation
- Yale University
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- Université de Fribourg
- Université de Lausanne
- Fondation Pierre Mercier
- Fondation Pierre Mercier pour la Science
- National Institutes of Health
- H2020 Marie Skłodowska-Curie Actions