Sex-specific, pdfr-1-dependent modulation of pheromone avoidance by food abundance enables flexibility in C. elegans foraging behavior

• Published in: Current biology Vol. 31; no. 20; pp. 4449 - 4461.e4
• Main Authors: Luo, Jintao, Portman, Douglas S.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 25-10-2021
• Subjects: Animals; ascarosides; behavior; C. elegans; Caenorhabditis elegans - genetics; Caenorhabditis elegans Proteins - genetics; Female; foraging; innate behavior; Male; neurogenetics; neuromodulation; pheromone; Pheromones; Sensory Receptor Cells - physiology; sex differences; Signal Transduction; Transcription Factors; neuromodulation; C. elegans; neurogenetics; innate behavior; foraging; pheromone; ascarosides; behavior; sex differences
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.07.069

To make adaptive feeding and foraging decisions, animals must integrate diverse sensory streams with multiple dimensions of internal state. In C. elegans, foraging and dispersal behaviors are influenced by food abundance, population density, and biological sex, but the neural and genetic mechanisms that integrate these signals are poorly understood. Here, by systematically varying food abundance, we find that chronic avoidance of the population-density pheromone ascr#3 is modulated by food thickness, such that hermaphrodites avoid ascr#3 only when food is scarce. The integration of food and pheromone signals requires the conserved neuropeptide receptor PDFR-1, as pdfr-1 mutant hermaphrodites display strong ascr#3 avoidance, even when food is abundant. Conversely, increasing PDFR-1 signaling inhibits ascr#3 aversion when food is sparse, indicating that this signal encodes information about food abundance. In both wild-type and pdfr-1 hermaphrodites, chronic ascr#3 avoidance requires the ASI sensory neurons. In contrast, PDFR-1 acts in interneurons, suggesting that it modulates processing of the ascr#3 signal. Although a sex-shared mechanism mediates ascr#3 avoidance, food thickness modulates this behavior only in hermaphrodites, indicating that PDFR-1 signaling has distinct functions in the two sexes. Supporting the idea that this mechanism modulates foraging behavior, ascr#3 promotes ASI-dependent dispersal of hermaphrodites from food, an effect that is markedly enhanced when food is scarce. Together, these findings identify a neurogenetic mechanism that sex-specifically integrates population and food abundance, two important dimensions of environmental quality, to optimize foraging decisions. Further, they suggest that modulation of attention to sensory signals could be an ancient, conserved function of pdfr-1.
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•Abundant food blocks hermaphrodite avoidance of a key population density pheromone•Food abundance is encoded by the conserved PDF/PDFR-1 neuropeptide system•PDFR-1 acts in interneurons to modulate the salience of the aversive pheromone cue•Food-pheromone integration allows value assessment and promotes adaptive foraging
To forage optimally, animals must predict the future value of an existing food resource. Here, Luo and Portman show that C. elegans can assess this by weighing food abundance against population density. The authors find that food abundance engages a conserved neuromodulatory pathway to modulate avoidance of a key population density pheromone.