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Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli

Abstract

Natural Caenorhabditis elegans isolates exhibit either social or solitary feeding on bacteria. We show here that social feeding is induced by nociceptive neurons that detect adverse or stressful conditions. Ablation of the nociceptive neurons ASH and ADL transforms social animals into solitary feeders. Social feeding is probably due to the sensation of noxious chemicals by ASH and ADL neurons; it requires the genes ocr-2 and osm-9, which encode TRP-related transduction channels, and odr-4 and odr-8, which are required to localize sensory chemoreceptors to cilia. Other sensory neurons may suppress social feeding, as social feeding in ocr-2 and odr-4 mutants is restored by mutations in osm-3, a gene required for the development of 26 ciliated sensory neurons. Our data suggest a model for regulation of social feeding by opposing sensory inputs: aversive inputs to nociceptive neurons promote social feeding, whereas antagonistic inputs from neurons that express osm-3 inhibit aggregation.

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Figure 1: Aggregation of npr-1 mutant animals requires food and is enhanced by increased population density and daf-7 TGF-β mutations.
Figure 2: Social feeding of npr-1 is lost in ocr-2, osm-9, odr-4 or odr-8 mutant backgrounds.
Figure 3: Mutations in ocr-2, osm-9, odr-4 and odr-8 restore the ability of npr-1 mutant animals to slow down upon encountering food.
Figure 4: The nociceptive neurons ASH and ADL are required for social feeding behaviour.
Figure 5: Disruption of osm-3 kinesin restores social feeding to mutants defective in nociceptive neuron function.

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Acknowledgements

We thank R. Cassada, who first observed aggregation behaviour in a wild isolate of C. elegans; D. Madsen and V. Maricq for making the ocr-2(ak47) allele available; Y. Zhang and E. Troemel for providing unpublished promoter constructs; A. Davies and S. McIntire for suggesting use of a physical barrier to limit nematode dispersal; A. Fire for expression plasmids; T. Stiernagle and the Caenorhabditis Genetics Center for C. elegans strains; and M. Hilliard, T. Reader, and J. Coates for suggestions and discussion during the course of this work. This work was supported by the Wellcome Trust, the Howard Hughes Medical Institute, and the Medical Research Council of Great Britain. C.I.B. is an investigator of the Howard Hughes Medical Institute.

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Correspondence to Mario de Bono.

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de Bono, M., Tobin, D., Davis, M. et al. Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419, 899–903 (2002). https://doi.org/10.1038/nature01169

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