Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-off

Abstract

Internal states can profoundly alter the behavior of animals. A quantitative understanding of the behavioral changes upon metabolic challenges is key to a mechanistic dissection of how animals maintain nutritional homeostasis. We used an automated video tracking setup to characterize how amino acid and reproductive states interact to shape exploitation and exploration decisions taken by adult Drosophila melanogaster. We find that these two states have specific effects on the decisions to stop at and leave proteinaceous food patches. Furthermore, the internal nutrient state defines the exploration-exploitation trade-off: nutrient-deprived flies focus on specific patches while satiated flies explore more globally. Finally, we show that olfaction mediates the efficient recognition of yeast as an appropriate protein source in mated females and that octopamine is specifically required to mediate homeostatic postmating responses without affecting internal nutrient sensing. Internal states therefore modulate specific aspects of exploitation and exploration to change nutrient selection.

DOI: http://dx.doi.org/10.7554/eLife.19920.001

eLife digest

When making decisions, animals, including humans, do not always choose the same option. One reason for this is that their “internal state” changes the value of different options. This is particularly evident when deciding what type of food to eat. Depending on which nutrients the animal needs, it will choose to eat different foods.

Amino acids are key nutrients that affect health, lifespan and reproduction. Female fruit flies that have recently mated, for example, eat more amino acids in order to obtain the raw materials required to produce eggs. Despite the importance of amino acids, little was known about how animal behavior changes in response to a lack of this nutrient.

Corrales-Carvajal et al. used a video tracking system to measure the time that fruit flies – some of which had a need for amino acids – spent feeding on patches of yeast (which are rich in amino acids) versus patches of sucrose. Recently mated females – and virgins that had been fed a diet lacking in amino acids – consumed more yeast than sucrose, whereas virgin females that were not amino acid deficient showed the opposite pattern. To bias the fly toward eating the right food for their needs, several aspects of the fly’s behavior changed, including the number and length of individual feeding bouts. These different behaviors did not all change at the same time.

The pattern of exploration taken by the flies also depended on their need for amino acids. Amino acid deficient flies spent most of their time near known yeast patches. By contrast, fully fed flies adopted a riskier foraging strategy, moving away from known sources of food to explore their environment more widely. In common with humans, the flies relied upon their sense of smell to efficiently identify different types of food.

Overall, the results presented by Corrales-Carvajal et al. provide us with a detailed understanding about how changes to the internal state of the fly affect its behavior. The next step will be to use the powerful genetic tools available for studying fruit flies to reveal the neural circuits and molecular mechanisms that help animals find the types of food that they need.

DOI: http://dx.doi.org/10.7554/eLife.19920.002