Abstract
Animals integrate external cues with information about internal conditions such as metabolic state to execute the appropriate behavioral and developmental decisions. Information about food quality and quantity is assessed by the intestine and transmitted to modulate neuronal functions via mechanisms that are not fully understood. The conserved Target of Rapamycin complex 2 (TORC2) controls multiple processes in response to cellular stressors and growth factors. Here we show that TORC2 coordinates larval development and adult behaviors in response to environmental cues and feeding state in the bacterivorous nematode C. elegans. During development, pheromone, bacterial food, and temperature regulate expression of the daf-7 TGF-β and daf-28 insulin-like peptide in sensory neurons to promote a binary decision between reproductive growth and entry into the alternate dauer larval stage. We find that TORC2 acts in the intestine to regulate neuronal expression of both daf-7 and daf-28, which together reflect bacterial-diet dependent feeding status, thus providing a mechanism for integration of food signals with external cues in the regulation of neuroendocrine gene expression. In the adult, TORC2 similarly acts in the intestine to modulate food-regulated foraging behaviors via a PDF-2/PDFR-1 neuropeptide signaling-dependent pathway. We also demonstrate that genetic variation affects food-dependent larval and adult phenotypes, and identify quantitative trait loci (QTL) associated with these traits. Together, these results suggest that TORC2 acts as a hub for communication of feeding state information from the gut to the brain, thereby contributing to modulation of neuronal function by internal state.
Highlights
Animals integrate complex and varying environmental stimuli in the context of their past experience and current conditions to execute the appropriate developmental and behavioral response
Information about the environment is obtained via the sensory nervous system, whereas internal state can be assessed via cues such as levels of hormones or nutrients
Via analyses of dauer formation and adult foraging behavior in C. elegans wild isolates, we show that these traits are genetically separable, and identify quantitative trait loci (QTL) that contribute to trait variation between two strains
Summary
Animals integrate complex and varying environmental stimuli in the context of their past experience and current conditions to execute the appropriate developmental and behavioral response. Nutritional experience regulates developmental trajectories and behavioral decisions, and modulates physiological state across phyla [1,2,3,4,5]. The importance of gut-to-brain signaling in the regulation of both developmental and behavioral traits has been demonstrated in several systems, and a subset of the underlying biochemical pathways has been identified [11,12,13,14,15,16,17]. How nutrient status is assessed and integrated with other cues to modulate development and behavior remains to be fully described
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