Sex, Age, and Hunger Regulate Behavioral Prioritization through Dynamic Modulation of Chemoreceptor Expression

• Published in: Current biology Vol. 24; no. 21; pp. 2509 - 2517
• Main Authors: Ryan, Deborah A., Miller, Renee M., Lee, KyungHwa, Neal, Scott J., Fagan, Kelli A., Sengupta, Piali, Portman, Douglas S.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 03-11-2014
• Subjects: Adaptation, Physiological; Animals; Behavior, Animal; Caenorhabditis elegans - metabolism; Caenorhabditis elegans - physiology; Chemoreceptor Cells - metabolism; Female; Hunger; Male; Sex Factors; Sexual Behavior, Animal; Time Factors
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2014.09.032

Adaptive behavioral prioritization requires flexible outputs from fixed neural circuits. In C. elegans, the prioritization of feeding versus mate searching depends on biological sex (males will abandon food to search for mates, whereas hermaphrodites will not) as well as developmental stage and feeding status. Previously, we found that males are less attracted than hermaphrodites to the food-associated odorant diacetyl, suggesting that sensory modulation may contribute to behavioral prioritization.
We show that somatic sex acts cell autonomously to reconfigure the olfactory circuit by regulating a key chemoreceptor, odr-10, in the AWA neurons. Moreover, we find that odr-10 has a significant role in food detection, the regulation of which contributes to sex differences in behavioral prioritization. Overexpression of odr-10 increases male food attraction and decreases off-food exploration; conversely, loss of odr-10 impairs food taxis in both sexes. In larvae, both sexes prioritize feeding over exploration; correspondingly, the sexes have equal odr-10 expression and food attraction. Food deprivation, which transiently favors feeding over exploration in adult males, increases male food attraction by activating odr-10 expression. Furthermore, the weak expression of odr-10 in well-fed adult males has important adaptive value, allowing males to efficiently locate mates in a patchy food environment.
We find that modulated expression of a single chemoreceptor plays a key role in naturally occurring variation in the prioritization of feeding and exploration. The convergence of three independent regulatory inputs—somatic sex, age, and feeding status—on chemoreceptor expression highlights sensory function as a key source of plasticity in neural circuits.
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•Somatic sex of the C. elegans AWA neurons regulates the diacetyl chemoreceptor ODR-10•ODR-10 has a prominent role in mediating food attraction•Low ODR-10 in males reduces food attraction and promotes mate searching•Sex, age, and hunger converge on sensory function to guide adaptive behavioral choice
In C. elegans, well-fed adult males prioritize mate searching, whereas hermaphrodites, larval males, and starved adult males prioritize feeding. Here, Ryan et al. show that sensory plasticity is central to this decision. By targeting a key chemoreceptor, sex, age, and hunger regulate food attraction to guide adaptive behavioral plasticity.