Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

An internal thermal sensor controlling temperature preference in Drosophila

Abstract

Animals from flies to humans are able to distinguish subtle gradations in temperature and show strong temperature preferences1,2,3,4. Animals move to environments of optimal temperature and some manipulate the temperature of their surroundings, as humans do using clothing and shelter. Despite the ubiquitous influence of environmental temperature on animal behaviour, the neural circuits and strategies through which animals select a preferred temperature remain largely unknown. Here we identify a small set of warmth-activated anterior cell (AC) neurons located in the Drosophila brain, the function of which is critical for preferred temperature selection. AC neuron activation occurs just above the fly’s preferred temperature and depends on dTrpA1, an ion channel that functions as a molecular sensor of warmth. Flies that selectively express dTrpA1 in the AC neurons select normal temperatures, whereas flies in which dTrpA1 function is reduced or eliminated choose warmer temperatures. This internal warmth-sensing pathway promotes avoidance of slightly elevated temperatures and acts together with a distinct pathway for cold avoidance to set the fly’s preferred temperature. Thus, flies select a preferred temperature by using a thermal sensing pathway tuned to trigger avoidance of temperatures that deviate even slightly from the preferred temperature. This provides a potentially general strategy for robustly selecting a narrow temperature range optimal for survival.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: dTrpA1 is required for warmth avoidance.
Figure 2: AC neurons are thermosensors.
Figure 3: AC neurons are necessary for warmth avoidance.
Figure 4: dTrpA1 is a warmth sensor.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The sequence for agTrpA1 has been deposited in the GenBank database under accession number EU624401.

References

  1. Fraenkel, G. & Gunn, D. The Orientation of Animals. Kineses, Taxes and Compass Relations (Clarendon, Oxford, 1940)

    Google Scholar 

  2. Fanger, P. O., Ostberg, O., Nicholl, A., Breum, N. O. & Jerking, E. Thermal comfort conditions during day and night. Eur. J. Appl. Physiol. 33, 255–263 (1974)

    Article  CAS  Google Scholar 

  3. Sayeed, O. & Benzer, S. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl Acad. Sci. USA 93, 6079–6084 (1996)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  4. Mori, I. Genetics of chemotaxis and thermotaxis in the nematode Caenorhabditis elegans. Annu. Rev. Genet. 33, 399–422 (1999)

    Article  CAS  PubMed  Google Scholar 

  5. Dhaka, A., Viswanath, V. & Patapoutian, A. TRP ion channels and temperature sensation. Annu. Rev. Neurosci. 29, 135–161 (2006)

    Article  CAS  PubMed  Google Scholar 

  6. Rosenzweig, M. et al. The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev. 19, 419–424 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Viswanath, V. et al. Opposite thermosensor in fruitfly and mouse. Nature 423, 822–823 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  8. Siddiqui, W. H. & Barlow, C. A. Population growth of Drosophila melanogaster (Dipetera:Drosophilidae) at constant and alternating temperatures. Ann. Entomol. Soc. Am. 65, 993–1001 (1972)

    Article  Google Scholar 

  9. Nakai, J., Ohkura, M. & Imoto, K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nature Biotechnol. 19, 137–141 (2001)

    Article  CAS  Google Scholar 

  10. Fischer, H. & Tichy, H. Cold-receptor cells supply both cold- and warm-responsive projection neurons in the antennal lobe of the cockroach. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 188, 643–648 (2002)

    Article  CAS  PubMed  Google Scholar 

  11. Vosshall, L. B. & Stocker, R. F. Molecular architecture of smell and taste in Drosophila. Annu. Rev. Neurosci. 30, 505–533 (2007)

    Article  CAS  PubMed  Google Scholar 

  12. Ito, K. et al. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52–77 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Kitamoto, T., Ikeda, K. & Salvaterra, P. M. Regulation of choline acetyltransferase/lacZ fusion gene expression in putative cholinergic neurons of Drosophila melanogaster. J. Neurobiol. 28, 70–81 (1995)

    Article  CAS  PubMed  Google Scholar 

  14. Brown, A. W. A. Factors in the attractives of bodies for mosquitoes. Nature 167, 202 (1951)

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Friend, W. G. & Smith, J. J. B. Factors affecting feeding by bloodsucking insects. Annu. Rev. Entomol. 22, 309–331 (1977)

    Article  CAS  PubMed  Google Scholar 

  16. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003)

    Article  ADS  CAS  PubMed  Google Scholar 

  17. Patapoutian, A., Peier, A. M., Story, G. M. & Viswanath, V. ThermoTRP channels and beyond: mechanisms of temperature sensation. Nature Rev. Neurosci. 4, 529–539 (2003)

    Article  CAS  Google Scholar 

  18. Tominaga, M. & Caterina, M. J. Thermosensation and pain. J. Neurobiol. 61, 3–12 (2004)

    Article  PubMed  Google Scholar 

  19. Tichy, H. & Gingl, E. Problems in hygro- and thermoreception. In The Ecology of Sensing (eds Barth, F. G. & Schimd, A.) 271–287 (Springer, New York, 2001)

    Chapter  Google Scholar 

  20. Liu, L., Yermolaieva, O., Johnson, W. A., Abboud, F. M. & Welsh, M. J. Identification and function of thermosensory neurons in Drosophila larvae. Nature Neurosci. 6, 267–273 (2003)

    Article  CAS  PubMed  Google Scholar 

  21. Stevenson, R. D. Body size and limits to the daily range of body temperature in terrestrial ectotherms. Am. Nat. 125, 102–117 (1985)

    Article  Google Scholar 

  22. Heinrich, B. The Hot-Blooded Insects: Strategies and Mechanisms of Thermoregulation (Harvard Univ. Press, Cambridge, USA, 1993)

    Book  Google Scholar 

  23. Caterina, M. J. Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R64–R76 (2007)

    Article  CAS  PubMed  Google Scholar 

  24. Barolo, S., Castro, B. & Posakony, J. W. New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP. Biotechniques 36, 436–440,–442 (2004)

    Article  Google Scholar 

  25. Rong, Y. S. & Golic, K. G. Gene targeting by homologous recombination in Drosophila. Science 288, 2013–2018 (2000)

    Article  ADS  CAS  PubMed  Google Scholar 

  26. Kalidas, S. & Smith, D. P. Novel genomic cDNA hybrids produce effective RNA interference in adult Drosophila. Neuron 33, 177–184 (2002)

    Article  CAS  PubMed  Google Scholar 

  27. Tayler, T. D., Robichaux, M. B. & Garrity, P. A. Compartmentalization of visual centers in the Drosophila brain requires Slit and Robo proteins. Development 131, 5935–5945 (2004)

    Article  CAS  PubMed  Google Scholar 

  28. Ng, M. et al. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36, 463–474 (2002)

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Garrity laboratory members and L. Griffith, L. Huang, R. Huey, E. Marder, C. Miller, M. Rosbash, P. Sengupta, G. Turrigiano and their laboratories for advice and manuscript comments. Supported by NINDS (PO1 NS044232, P30 NS045713S10 and RR16780), NEI (RO1 EY13874, P.A.G.), NIMH (RO1 MH067284, to L. Griffith (for S.P. and A.G.)), and Japan Society for the Promotion of Science (F.N.H.)

Author Contributions F.N.H., M.R., S.R.P., K.K. and P.A.G. designed experiments; F.N.H. performed behaviour and imaging; M.R. created the dTrpA1 mutant, Gal4, RNAi and rescue strains; K.K. performed oocyte electrophysiology and dTrpA1 overexpression; S.R.P. performed NMJ electrophysiology, A.G. assisted with imaging; T.J.J. isolated agTrpA1 cDNA; and P.A.G. performed bioinformatics and assisted with knockdown studies. F.N.H. and P.A.G. wrote the paper with assistance from M.R., K.K., S.R.P. and A.G.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul A. Garrity.

Supplementary information

Supplementary Figures

The file contains Supplementary Figures 1-7 with Legends. (PDF 6902 kb)

Supplementary Movie

The file contains Supplementary Movie 1. Flies that express dTRPA1 in all neurons (c155-Gal4;UAS-dTRPA1; right-hand vial) were temporarily incapacitated by heating to 35°C for 60 seconds, while control flies (which contain only the c155-Gal4 source or the UAS-dTRPA1 transgene alone; left-hand and middle vials, respectively) were not. All flies were heated by submerging their vials in a 35°C water bath for 60 seconds. Heat treatment was done off camera. Some empty frames recorded during heat treatment were removed. The movie is accelerated 8-fold. (MOV 2595 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hamada, F., Rosenzweig, M., Kang, K. et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217–220 (2008). https://doi.org/10.1038/nature07001

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature07001

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing