Conserved autism-associated genes tune social feeding behavior inC. elegans

Abstract

Animal foraging is an essential and evolutionarily conserved behavior that occurs in social and solitary contexts, but the underlying molecular pathways are not well defined. We discover that conserved autism-associated genes (NRXN1(nrx-1),NLGN3(nlg-1),GRIA1,2,3(glr-1),GRIA2(glr-2), andGLRA2,GABRA3(avr-15))regulate aggregate feeding inC. elegans, a simple social behavior. NRX-1 functions in chemosensory neurons (ADL and ASH) independently of its postsynaptic partner NLG-1 to regulate social feeding. Glutamate from these neurons is also crucial for aggregate feeding, acting independently of NRX-1 and NLG-1. Compared to solitary counterparts, social animals show faster presynaptic release and more presynaptic release sites in ASH neurons, with only the latter requiringnrx-1. Disruption of these distinct signaling components additively converts behavior from social to solitary. Aggregation induced by circuit activation is also dependent onnrx-1. Collectively, we find that aggregate feeding is tuned by conserved autism-associated genes through complementary synaptic mechanisms, revealing molecular principles driving social feeding.TEASERConserved autism-associated genes mediate distinct molecular and circuit signaling components that cooperate to tuneC. eleganssocial feeding behavior.