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Distinct activity-gated pathways mediate attraction and aversion to CO₂ in Drosophila

van Breugel, Floris and Huda, Ainul and Dickinson, Michael H. (2018) Distinct activity-gated pathways mediate attraction and aversion to CO₂ in Drosophila. Nature, 564 (7736). pp. 420-424. ISSN 0028-0836. PMCID PMC6314688. https://resolver.caltech.edu/CaltechAUTHORS:20181002-123800797

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[img] Image (JPEG) (Extended Data Fig. 1: Drosophila prefer early fermentations, at peak CO_2 production) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 2: Responses of flies to odours at different concentrations) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 3: Walking arena geometry and odour stimulus) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 4: Responses to CO_2 are strongest at 5% concentration and are unaffected by social dynamics) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 5: Temperature measurements in the walking arena show no correlation with CO_2 or clean air stimuli) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 6: Flies do not respond to a stimulus of clean air (without CO_2)) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 7: IR25a is required for CO_2 attraction and IR40a is not) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 8: IR25a is required for ethanol attraction but not vinegar attraction) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 9: Drosophila are attracted to fatal levels of CO_2) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 10: Flies and mosquitoes both increase CO_2 production when shaken) - Supplemental Material
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[img] PDF (statistics and reproducibility data and a discussion of the effects of CO_2 concentration) - Supplemental Material
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[img] Video (QuickTime) (Video 1. Drosophila find CO_2 aversive during periods of low activity) - Supplemental Material
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[img] Video (QuickTime) (Video 2. Drosophila find CO_2 attractive during periods of high activity) - Supplemental Material
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[img] Video (QuickTime) (Video 3. Drosophila’s response to CO_2 during high activity is qualitatively similar to their response towards ethanol) - Supplemental Material
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Abstract

Carbon dioxide is produced by many organic processes and is a convenient volatile cue for insects that are searching for blood hosts, flowers, communal nests, fruit and wildfires. Although Drosophila melanogaster feed on yeast that produce CO₂ and ethanol during fermentation, laboratory experiments suggest that walking flies avoid CO₂. Here we resolve this paradox by showing that both flying and walking Drosophila find CO₂ attractive, but only when they are in an active state associated with foraging. Their aversion to CO₂ at low-activity levels may be an adaptation to avoid parasites that seek CO₂, or to avoid succumbing to respiratory acidosis in the presence of high concentrations of CO_2 that exist in nature. In contrast to CO₂, flies are attracted to ethanol in all behavioural states, and invest twice the time searching near ethanol compared to CO₂. These behavioural differences reflect the fact that ethanol is a unique signature of yeast fermentation, whereas CO₂ is generated by many natural processes. Using genetic tools, we determined that the evolutionarily conserved ionotropic co-receptor IR25a is required for CO₂ attraction, and that the receptors necessary for CO₂ avoidance are not involved in this attraction. Our study lays the foundation for future research to determine the neural circuits that underlie both state- and odorant-dependent decision-making in Drosophila.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41586-018-0732-8DOIArticle
https://doi.org/10.1101/227991DOIDiscussion Paper
https://rdcu.be/bbHeiPublisherFree ReadCube access
https://doi.org/10.5061/dryad.2s8422fDOIProcessed data
https://github.com/florisvb/drosophila_co2_attractionRelated ItemCode
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6314688PubMed CentralArticle
ORCID:
AuthorORCID
van Breugel, Floris0000-0001-6538-7179
Huda, Ainul0000-0003-2073-6659
Dickinson, Michael H.0000-0002-8587-9936
Alternate Title:Distinct activity-gated pathways mediate attraction and aversion to CO2 in Drosophila, Drosophila have distinct activity-gated pathways that mediate attraction and aversion to CO2
Additional Information:© 2018 Springer Nature Limited. Received: 22 December 2017; Accepted: 11 October 2018; Published online: 21 November 2018. We thank A. Straw for the 3D tracking software. Several colleagues provided mutants: R. Benton (quadruple mutant), R. Stanewsky (IR25a and rescue); G. Suh (IR8a); and M. Gallio and M. Stensmyr (IR40a). R. Benton, E. Hong and J. Riffell contributed helpful comments. This work was funded by grants from NIH (NIH1RO1DCO13693-01, U01NS090514) and the Simons Foundation. Reviewer information: Nature thanks S. Combes, M. Frye, L. Vosshall and R. Wilson for their contribution to the peer review of this work. Author Contributions: F.v.B. and M.H.D. conceived the experiments. A.H. made genetic recombinants. F.v.B. and A.H. performed experiments. F.v.B. analysed data. F.v.B. and M.H.D. wrote the manuscript. Data availability: Processed data are available in a Dryad repository at https://doi.org/10.5061/dryad.2s8422f. Raw data are available from the corresponding author upon request. Code availability: Custom code is available online at https://github.com/florisvb/drosophila_co2_attraction. Reporting summary: Further information on research design is available in the Nature Research Reporting Summary linked to this paper. The authors declare no competing interests.
Funders:
Funding AgencyGrant Number
NIH1RO1DCO13693-01
NIHU01NS090514
Simons FoundationUNSPECIFIED
Issue or Number:7736
PubMed Central ID:PMC6314688
Record Number:CaltechAUTHORS:20181002-123800797
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20181002-123800797
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:90085
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:08 Oct 2018 22:29
Last Modified:21 Jan 2020 17:15

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