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Inversion of pheromone preference optimizes foraging in C. elegans

M. Dal Bello, View ORCID ProfileA. Pérez-Escudero, F. C. Schroeder, View ORCID ProfileJ. Gore
doi: https://doi.org/10.1101/2020.05.18.101352
M. Dal Bello
1Physics of Living Systems Group, Department of Physics, Massachusetts Institute of Technology, 02139 Cambridge, Massachusetts, United States
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  • For correspondence: dalbello@mit.edu gore@mit.edu
A. Pérez-Escudero
1Physics of Living Systems Group, Department of Physics, Massachusetts Institute of Technology, 02139 Cambridge, Massachusetts, United States
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  • ORCID record for A. Pérez-Escudero
F. C. Schroeder
2Boyce Thompson Institute and Department of Chemistry and Chemical Biology, Cornell University, 14853 Ithaca, New York, United States
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J. Gore
1Physics of Living Systems Group, Department of Physics, Massachusetts Institute of Technology, 02139 Cambridge, Massachusetts, United States
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  • For correspondence: dalbello@mit.edu gore@mit.edu
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Summary

Foraging animals have to locate food sources that are usually patchily distributed and subject to competition. Deciding when to leave a food patch is challenging and requires the animal to integrate information about food availability with cues signaling the presence of other individuals (e.g. pheromones). To study how social information transmitted via pheromones can aid foraging decisions, we investigated the behavioral responses of the model nematode Caenorhabditis elegans to food depletion and pheromone accumulation in food patches. We experimentally show that animals consuming a food patch leave it at different times and that the leaving time affects the animal preference for its pheromones. In particular, worms leaving early are attracted to their pheromones, while worms leaving later are repelled by them. We further demonstrate that the inversion from attraction to repulsion depends on associative learning and, by implementing a simple model, we highlight that it is an adaptive solution to optimize food intake during foraging.

Footnotes

  • Lead contact: Jeff Gore gore{at}mit.edu

  • ↵1 In general, we have g(t) = Cai(t), where C is a constant. But we simply amounts to re-scaling the units of time).

  • ↵2 2 Proof: If mi worms occupy a patch, and each worm feeds at a rat a rate Embedded Image. Assuming that mi remains constant over time, the a(t) = A0e−mt, where A0 is the initial food density.

  • ↵3 Proof: Embedded Image. This is always negative as long as A > gD, because N is always positive and all terms inside the sum are squared.

  • ↵4 We assume that the population is large enough so that a single mutant does not alter the distributions significantly.

  • ↵5 Proof: Embedded Image, where Δni is defined as in Equation (3), and we define Embedded Image. We will show first that Δni and αi are perfectly anticorrelated (i.e. if Δni > Δnj, then αi < αj for any i, j). Then, we will show that this implies that Embedded Image must be negative.

    Δni and αi are perfectly anticorrelated: Both Δni and αi depend on ni. Let’s see that their derivatives with respect to it have opposite signs: From Equation (3), Embedded Image, so it’s positive. From Equation (1), Embedded Image, so Embedded Image has the same sign as Embedded Image. Given that Embedded Image and Embedded Image are always positive, this has the same sign as Embedded Image Embedded Image, which is always negative (it’s zero for mi = 0, and Embedded Image as long as tS ≥ 0 and mi ≥ 0, which is always true. Therefore, Embedded Image is always negative.

    Embedded Image is always negative: Let’s split the sum, separating the terms according to the sign of Δni: Embedded Image. Now, given that all the Δni in the first sum are greater than all the Δni in the second, and that Δni and αi are perfectly anticorrelated, all the αi in the first sum must be smaller than all the αi in the second. Therefore, we can find a number α0 which is in the middle of the two groups of αi, so that Embedded Image,

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted May 21, 2020.
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Inversion of pheromone preference optimizes foraging in C. elegans
M. Dal Bello, A. Pérez-Escudero, F. C. Schroeder, J. Gore
bioRxiv 2020.05.18.101352; doi: https://doi.org/10.1101/2020.05.18.101352
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Inversion of pheromone preference optimizes foraging in C. elegans
M. Dal Bello, A. Pérez-Escudero, F. C. Schroeder, J. Gore
bioRxiv 2020.05.18.101352; doi: https://doi.org/10.1101/2020.05.18.101352

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