Neuronal and molecular substrates for optimal foraging in Caenorhabditis elegans

Abstract

Variation in food quality and abundance requires animals to decide whether to stay on a poor food patch or leave in search of better food. An important question in behavioral ecology asks when is it optimal for an animal to leave a food patch it is depleting. Although optimal foraging is central to evolutionary success, the neural and molecular mechanisms underlying it are poorly understood. Here we investigate the neuronal basis for adaptive food-leaving behavior in response to resource depletion in Caenorhabditis elegans, and identify several of the signaling pathways involved. The ASE neurons, previously implicated in salt chemoattraction, promote food-leaving behavior via a cGMP pathway as food becomes limited. High ambient O 2 promotes foodleaving via the O 2 -sensing neurons AQR, PQR, and URX. Ectopic activation of these neurons using channelrhodopsin is sufficient to induce high food-leaving behavior. In contrast, the neuropeptide receptor NPR-1, which regulates social behavior on food, acts in the ASE neurons, the nociceptive ASH neurons, and in the RMG interneuron to repress food-leaving. Finally, we show that neuroendocrine signaling by TGF-β/DAF-7 and neuronal insulin signaling are necessary for adaptive food-leaving behavior. We suggest that animals integrate information about their nutritional state with ambient oxygen and gustatory stimuli to formulate optimal foraging strategies.food-leaving decision | Marginal Value Theorem | sensory neurons

Dynamic switching between escape and avoidance regimes reduces Caenorhabditis elegans exposure to noxious heat

“…By this mean, worms favour efficient heat avoidance mechanisms when they are within innocuous temperatures and favour efficient escape mechanisms when they are exposed to noxious heat. This behavioural transition presents some similarities with the local search/dispersal behavioural switch observed following food deprivation 33 and to the dwelling/roaming switches regulated by the quality of food and associated with optimal foraging strategies [34][35][36] . Thus, changing the behavioural rules according to environmental inputs is not only important to improve foraging and exploratory behaviours, but also help minimizing the exposure to noxious heat.…”

Farming and public goods production in Caenorhabditis elegans populations

“…1A). Because the bacterial strain we use is nonmotile, the worm's movement within and outside of the initial patch of bacteria (34,35) is responsible for redistributing the bacterial resource.…”

Molecular evolution of peptidergic signaling systems in bilaterians

“…We found several examples of orthologous neuromodulatory systems in mammals and ecdysozoans that could be involved in orthologous circuits. Neuromodulation by noradrenaline in the mammalian brain and of tyramine and octopamine in the insect brain is responsible for the specification of an arousal state which sets off "flight or fight" behavioral responses (52), whereas signaling of dopamine and NPY/NPF in mammals and ecdysozoans participates in defining robust hunger states that qualitatively affect the response to food stimuli (53)(54)(55). Other examples of functional analogy between orthologous protostome and deuterostome PSs include the cholecystokinin/sulfakinin that are involved in satiety (22) in humans and worms, and GnRH and AKH that have analogous functions in reproduction in both humans and worms (20).…”