Abstract
Insulin signalling plays a significant role in both developmental programmes and pathways modulating the neuronal signalling that controls adult behaviour. Here, we have investigated insulin signalling in food-associated behaviour in adult C. elegans by scoring locomotion and feeding on and off bacteria, the worm’s food. This analysis used mutants (daf-2, daf-18) of the insulin signalling pathway, and we provide evidence for an acute role for insulin signalling in the adult nervous system distinct from its impact on developmental programmes. Insulin receptor daf-2 mutants move slower than wild type both on and off food and showed impaired locomotory responses to food deprivation. This latter behaviour is manifest as a failure to instigate dispersal following prolonged food deprivation and suggests a role for insulin signalling in this adaptive response. Insulin receptor daf-2 mutants are also deficient in pharyngeal pumping on food and off food. Pharmacological analysis showed the pharynx of daf-2 is selectively compromised in its response to 5-HT compared to the excitatory neuropeptide FLP-17. By comparing the adaptive pharyngeal behaviour in intact worms and isolated pharyngeal preparations, we determined that an insulin-dependent signal extrinsic to the pharyngeal system is involved in feeding adaptation. Hence, we suggest that reactive insulin signalling modulates both locomotory foraging and pharyngeal pumping as the animal adapts to the absence of food. We discuss this in the context of insulin signalling directing a shift in the sensitivity of neurotransmitter systems to regulate the worm’s response to changes in food availability in the environment.
Highlights
An animal must be capable of adapting multiple behaviours in response to changes in its metabolic and nutritional status (Friedman 2010)
This analysis used mutants of the insulin signalling pathway, and we provide evidence for an acute role for insulin signalling in the adult nervous system distinct from its impact on developmental programmes
The strong daf-2 mutants moved at a slower speed at 60-min off food compared to 5-min off food [*59 % decrease for daf-2(e1370) and 100 % for daf-2(e979)]
Summary
An animal must be capable of adapting multiple behaviours in response to changes in its metabolic and nutritional status (Friedman 2010). Presentation of food triggers sensory inputs that drive an increased pumping that draws bacteria into the gut This integrative response involves several transmitter pathways but is largely dependent of 5-HT, acetylcholine and neuropeptides (Franks et al 2006; Dalliere et al 2016). Further evidence for a shifting tone in pharyngeal pumping comes from observations that show a sensitization of the pharynx to food exposure subsequent to the protracted incubation to periods off food (Avery and Horvitz 1990; Lemieux et al 2015) Taken together, these observations indicate complex regulation of food-dependent pharyngeal behaviours in which the intrinsic and extrinsic pharyngeal nervous system is involved
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