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Catecholamine receptor polymorphisms affect decision-making in C. elegans

Nature volume 472, pages 313–318 (2011)Cite this article

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Abstract

Innate behaviours are flexible: they change rapidly in response to transient environmental conditions, and are modified slowly by changes in the genome. A classical flexible behaviour is the exploration–exploitation decision, which describes the time at which foraging animals choose to abandon a depleting food supply. We have used quantitative genetic analysis to examine the decision to leave a food patch in Caenorhabditis elegans. Here we show that patch-leaving is a multigenic trait regulated in part by naturally occurring non-coding polymorphisms in tyra-3 (tyramine receptor 3), which encodes a G-protein-coupled catecholamine receptor related to vertebrate adrenergic receptors. tyra-3 acts in sensory neurons that detect environmental cues, suggesting that the internal catecholamines detected by tyra-3 regulate responses to external conditions. These results indicate that genetic variation and environmental cues converge on common circuits to regulate behaviour, and suggest that catecholamines have an ancient role in regulating behavioural decisions.

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Figure 1: Lawn-leaving behaviour varies between wild-type C. elegans strains.
Figure 2: N2 and HW tyra-3 alleles differentially affect leaving rates.
Figure 3: Non-coding changes in tyra-3 affect its activity and expression level.
Figure 4: tyra-3 acts in ASK and BAG sensory neurons.

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Acknowledgements

We thank R. Shingai for strains, and P. McGrath and members of the C.I.B. laboratory for discussions. A.B. was supported by the Secretaría de Educación Pública of Mexico and by The Rockefeller University. C.I.B. and L.K. are Investigators of the Howard Hughes Medical Institute. This work was supported by HHMI and by NIH grant GM089972.

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Authors and Affiliations

  1. Howard Hughes Medical Institute, Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, 10065, New York, USA

    Andres Bendesky, Makoto Tsunozaki & Cornelia I. Bargmann

  2. Department of Biology and Center for Genomics and Systems Biology, New York University, New York, 10003, New York, USA

    Matthew V. Rockman

  3. Lewis-Sigler Institute for Integrative Genomics and Department of Ecology and Evolutionary Biology, Howard Hughes Medical Institute, Carl Icahn Laboratory, Princeton University, Princeton, 08544, New Jersey, USA

    Leonid Kruglyak

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Contributions

A.B. and C.I.B. designed experiments, A.B. conducted experiments, M.V.R. constructed strains for QTL mapping, M.T. developed tracking methods, A.B., M.V.R., L.K. and C.I.B. analysed and interpreted results, and A.B. and C.I.B. wrote the paper.

Corresponding author

Correspondence to Cornelia I. Bargmann.

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Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-10 with legends, Supplementary Table 1, Supplementary Methods, Strain List and additional references. (PDF 6105 kb)

Supplementary Movie 1

This movie shows leaving assay showing six N2 adults, 20x actual speed. The border of the bacterial lawn is outlined for ease of visualization. Time stamp at upper left displays the actual time after placing the animals on the assay plate. (MOV 8791 kb)

Supplementary Movie 2

This movie shows leaving assay showing six HW adults, 20x actual speed. Four animals are on the lawn and two off the lawn at the beginning of the assay. The border of the bacterial lawn is outlined for ease of visualization. Time stamp at upper left displays the actual time after placing the animals on the assay plate. (MOV 8791 kb)

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Bendesky, A., Tsunozaki, M., Rockman, M. et al. Catecholamine receptor polymorphisms affect decision-making in C. elegans. Nature 472, 313–318 (2011). https://doi.org/10.1038/nature09821

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