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

Dietary choices are influenced by genotype, mating status, and sex in Drosophila melanogaster

“…For females, our findings echo previously obtained results (Corrales‐Carvajal et al., 2016; Ribeiro & Dickson, 2010; Vargas et al., 2010). We found a significant mating response, with mated females consuming more protein and carbohydrate than virgin females.…”

“…For this reason, we would rather have a more conservative approach and exclude carbohydrate measures. We also note that most dietary preference work in insects does not use a holidic diet, but rather yeast extract as the protein source (42% protein; Corrales‐Carvajal et al., 2016; Reddiex et al., 2013). Our diet thus provides an important step in the right direction and future work regarding the holidic medium should aim to identify the sensory cue that is missing from the protein source.…”

“…A metabolic shift can phenotypically manifest as a switch in requirement of certain macronutrients to meet the new nutritional demands of the organism. For example, several studies have examined dietary choices in flies, concluding that flies can actively make food choices according to their internal state in a sex‐specific manner (Corrales‐Carvajal, Faisal, & Ribeiro, 2016; Ribeiro & Dickson, 2010; Vargas, Luo, Yamaguchi, & Kapahi, 2010). Moreover, nutritional choices have been found to differ depending on the mating status of females.…”

“…Moreover, nutritional choices have been found to differ depending on the mating status of females. While virgin females mostly fed on carbohydrate‐based diets, mated females not only elevated their overall amount of food consumed (food quantity), but increased the concentration of protein ingested (food quality; Corrales‐Carvajal et al., 2016). In Drosophila females, egg production (reproductive output) has been directly linked to the nutritional state of female flies, with flies having a greater reproductive output on diets containing higher protein concentrations (Piper et al., 2014; Simmons & Bradley, 1997; Terashima & Bownes, 2004).…”

“…These results allude to both a metabolic and behavioral shift for diet preference in response to a change in reproductive requirements (Kubli, 2010). However, most studies that have examined dietary responses to mating have only used one sex (females), and thus, we do not know whether males go through a similar physiological change (Corrales‐Carvajal et al., 2016; Ribeiro & Dickson, 2010; Vargas et al., 2010). …”