Inversion of pheromone preference optimizes foraging in C. elegans
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Abstract
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.
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This manuscript is in revision at eLife
The decision letter after re-review, sent to the authors on February 2 2021, follows.
Summary
The reviewers concur that this article offers an interesting conclusion regarding optimal foraging and chemosensory valence. However, they also agree that it would benefit from a second round of revision, aiming at an improved precision of language and a better discussion of the assumptions of the model and experimental conclusions.
Public Review 1:
The authors present experiments that demonstrate how C. elegans worms bias their foraging decisions depending on feeding history and sensory cues (here, called pheromones) that reflect the density of worms. Navigational preference for these sensory cues is found to change from attractive to repulsive depending on the time at which worms leave a food patch, and …
This manuscript is in revision at eLife
The decision letter after re-review, sent to the authors on February 2 2021, follows.
Summary
The reviewers concur that this article offers an interesting conclusion regarding optimal foraging and chemosensory valence. However, they also agree that it would benefit from a second round of revision, aiming at an improved precision of language and a better discussion of the assumptions of the model and experimental conclusions.
Public Review 1:
The authors present experiments that demonstrate how C. elegans worms bias their foraging decisions depending on feeding history and sensory cues (here, called pheromones) that reflect the density of worms. Navigational preference for these sensory cues is found to change from attractive to repulsive depending on the time at which worms leave a food patch, and additional experiments that condition worms under different combinations of conditions (with/without the sensory cues, with/without food, with/without repellent) indicate that associative learning is involved in this inversion of preference. A mathematical model is provided to argue that this inversion represents an optimal foraging strategy that is also evolutionarily stable.
Public Review 2:
The authors use the nematode C. elegans to reveal how animals associate social signals with specific contexts and modify their behaviors. Specifically, they show that C. elegans leaving a food patch are attracted to pheromonal cues, while those leaving later are repelled from pheromones. The authors using a behavioral model to suggest that the switch from attraction to repulsion is likely due to a change in learning. This study links learning with social signals providing a framework for further analysis into the underlying neuronal pathways.
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