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

Abstract

Background Adaptive behavioral prioritization requires flexible outputs from fixed neural circuits. In C. elegans, the prioritization of feeding vs. mate-searching depends on biological sex (males will abandon food to search for mates, while 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. Results We find 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, odr-10 loss 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. Conclusions 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.

A natural odor attraction between lactic acid bacteria and the nematode Caenorhabditis elegans

“…In fact, we observe diacetyl receptor-independent attraction to LAB grown on barley, tomato and apple, indicating odors other than diacetyl are mediating attraction in these assays. Furthermore, a recent investigation has suggested the importance of the diacetyl receptor for C. elegans to sense E. coli bacteria, allowing males to make correct behavioral choices between eating and mating (Ryan et al, 2014). Attraction to diacetyl odor in C. remanei and the closely related nematode Caenorhabditis briggsae has been established (Hong and Sommer, 2006).…”

Wired for sex

“…In C. elegans, an individual's sex is determined by the number of X chromosomes it carries. Reversing this genetic signal in the nervous system -or even in individual neurons -has been shown to alter circuit physiology and behaviour 10 . Using this approach, the researchers found that the genetic sex of individual neurons can also determine whether a particular synapse is pruned.…”

Plasticity of chemoreceptor gene expression: Sensory and circuit inputs modulate state-dependent chemoreceptors

“…[10][11][12] As in other animals, dynamic changes in expression levels of chemoreceptor genes appear to directly alter chemosensory behaviors. For example, a recent study showed that altered expression level changes of the odr-10 chemoreceptor gene, known to sense the food-related chemical diacetyl, 13 modifies C. elegans male exploratory behavior 14 ( Fig. 1C).…”