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Distinct activity-gated pathways mediate attraction and aversion to CO_2 in Drosophila

van Breugel, Floris and Huda, Ainul and Dickinson, Michael H. (2018) Distinct activity-gated pathways mediate attraction and aversion to CO_2 in Drosophila. Nature, 564 (7736). pp. 420-424. ISSN 0028-0836. http://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] 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 CO_2 and ethanol during fermentation, laboratory experiments suggest that walking flies avoid CO_2. Here we resolve this paradox by showing that both flying and walking Drosophila find CO_2 attractive, but only when they are in an active state associated with foraging. Their aversion to CO_2 at low-activity levels may be an adaptation to avoid parasites that seek CO_2, or to avoid succumbing to respiratory acidosis in the presence of high concentrations of CO_2 that exist in nature. In contrast to CO_2, flies are attracted to ethanol in all behavioural states, and invest twice the time searching near ethanol compared to CO_2. These behavioural differences reflect the fact that ethanol is a unique signature of yeast fermentation, whereas CO_2 is generated by many natural processes. Using genetic tools, we determined that the evolutionarily conserved ionotropic co-receptor IR25a is required for CO_2 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
ORCID:
AuthorORCID
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
Record Number:CaltechAUTHORS:20181002-123800797
Persistent URL:http://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 Dec 2018 18:38

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