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Balancing selection shapes density-dependent foraging behaviour

Author

Listed:
  • Joshua S. Greene

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

  • Maximillian Brown

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

  • May Dobosiewicz

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

  • Itzel G. Ishida

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

  • Evan Z. Macosko

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

  • Xinxing Zhang

    (University of Florida)

  • Rebecca A. Butcher

    (University of Florida)

  • Devin J. Cline

    (School of Biological Sciences, Georgia Institute of Technology)

  • Patrick T. McGrath

    (School of Biological Sciences, Georgia Institute of Technology)

  • Cornelia I. Bargmann

    (Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University)

Abstract

The optimal foraging strategy in a given environment depends on the number of competing individuals and their behavioural strategies. Little is known about the genes and neural circuits that integrate social information into foraging decisions. Here we show that ascaroside pheromones, small glycolipids that signal population density, suppress exploratory foraging in Caenorhabditis elegans, and that heritable variation in this behaviour generates alternative foraging strategies. We find that natural C. elegans isolates differ in their sensitivity to the potent ascaroside icas#9 (IC-asc-C5). A quantitative trait locus (QTL) regulating icas#9 sensitivity includes srx-43, a G-protein-coupled icas#9 receptor that acts in the ASI class of sensory neurons to suppress exploration. Two ancient haplotypes associated with this QTL confer competitive growth advantages that depend on ascaroside secretion, its detection by srx-43 and the distribution of food. These results suggest that balancing selection at the srx-43 locus generates alternative density-dependent behaviours, fulfilling a prediction of foraging game theory.

Suggested Citation

  • Joshua S. Greene & Maximillian Brown & May Dobosiewicz & Itzel G. Ishida & Evan Z. Macosko & Xinxing Zhang & Rebecca A. Butcher & Devin J. Cline & Patrick T. McGrath & Cornelia I. Bargmann, 2016. "Balancing selection shapes density-dependent foraging behaviour," Nature, Nature, vol. 539(7628), pages 254-258, November.
  • Handle: RePEc:nat:nature:v:539:y:2016:i:7628:d:10.1038_nature19848
    DOI: 10.1038/nature19848
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    Cited by:

    1. Minjie Hong & Xiaotian Zhou & Chenming Zeng & Demin Xu & Ting Xu & Shimiao Liao & Ke Wang & Chengming Zhu & Ge Shan & Xinya Huang & Xiangyang Chen & Xuezhu Feng & Shouhong Guang, 2024. "Nucleolar stress induces nucleolar stress body formation via the NOSR-1/NUMR-1 axis in Caenorhabditis elegans," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Jacob D Davidson & Ahmed El Hady, 2019. "Foraging as an evidence accumulation process," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-25, July.

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