Gustatory and metabolic perception of nutrient stress in Drosophila

Abstract

Sleep loss is an adaptive response to nutrient deprivation that alters behavior to maximize the chances of feeding before imminent death. Organisms must maintain systems for detecting the quality of the food source to resume healthy levels of sleep when the stress is alleviated. We determined that gustatory perception of sweetness is both necessary and sufficient to suppress starvation-induced sleep loss when animals encounter nutrient-poor food sources. We further find that blocking specific dopaminergic neurons phenocopies the absence of gustatory stimulation, suggesting a specific role for these neurons in transducing taste information to sleep centers in the brain. Finally, we show that gustatory perception is required for survival, specifically in a low nutrient environment. Overall, these results demonstrate an important role for gustatory perception when environmental food availability approaches zero and illustrate the interplay between sensory and metabolic perception of nutrient availability in regulating behavioral state.tarvation is a condition of extreme nutrient stress that leads to rapid death. On detecting the absence of environmental nutrient sources, organisms use multiple strategies to adjust resource allocation to maximize the chances of finding a food source, including inducing longer foraging searches (1) and limiting sleep behavior (2, 3). Sleep loss in Drosophila melanogaster is a characteristic response to nutrient deprivation that appears ∼12 h after the removal of a food source; in males, it is followed by death in another 12 h (2). Sleep loss is thought to represent a cost to the organism (4-6), and mechanisms for evaluating the environment and terminating this behavioral response when food is available would likely confer an adaptive benefit. A deeper understanding of how organisms perceive and respond to environmental stress could offer substantial benefit to humans attempting to maintain maximal health in the face of food shortages and unstable environmental conditions. The strategies used by organisms to evaluate the sufficiency of a food source and to initiate or suppress sleep loss under very low nutrient conditions remain largely unknown and represent one path toward understanding global stress response. ResultsWe have observed, as previously reported, that adult Drosophila spontaneously adjust their behavioral patterns to reduce sleep when starved (Fig. 1A) (2, 7). To more completely understand how organisms modulate sleep in response to food availability, we measured the extent of nutrient deprivation required to induce sleep loss. These assays consist of monitoring the activity of male Canton-S flies on a complete medium (10% sugar:Brewer's yeast medium; Materials and Methods) for 1 d (day 1) to estimate baseline sleep in the fully fed condition, followed by data collection from 1 or more days on a 1% agar-only starvation medium (day 2+), which provides water and humidity but not nutrients. We modified this procedure by augmenting the agar medium with either 50 mM D-glucose ...

Starvation stress during larval development facilitates an adaptive response in adult worker honey bees (Apis mellifera L.)

“…Indeed, we found that larval starvation impacted adult feeding behavior, measured as the gustatory perception of sugar. Gustatory perception is critical for animal survival, perhaps especially in a low-nutrient environment (Linford et al, 2015), as it helps an organism locate energy-rich food sources in order to maintain adequate nutrition (Drewnowski, 2000;Rohwedder et al, 2012). In our study, we observed reduced gustatory perception in the adult bees that experienced starvation as larvae.…”

Dietary fatty acids promote sleep through a taste‐independent mechanism

“…Hexanoic acid and sugars are detected by shared peripheral sensory neurons that are also known to regulate sleep . Therefore, it is possible that fatty acids promote sleep by providing nutrients, or through the activation of these sensory neurons.…”

“…Dietary nutrients can be perceived via peripheral processing by the taste system as well as by taste‐independent mechanisms . In the taste system, thermogenetically activating sweet sensing neurons labeled by the Gustatory receptor 64f is sufficient to restore normal sleep to starved flies . However, whether flies lacking sugar receptors suppress sleep on an all sugar diet have been conflicting .…”

“…Food is comprised of complex macronutrients including sugars, proteins and fats. In flies, diet composition has been shown to impact sleep, but studies have primarily relied upon varying the concentrations of sugars and protein, or fully food‐restricting animals . Flies are capable of tasting a number of additional compounds including fatty acids, salt, amino acids and carbonation, but the effects of these factors on sleep regulation has not been explored.…”

Dietary fatty acids promote sleep through a taste-independent mechanism

“…Food is comprised of complex macronutrients including sugars, proteins, and fats. In flies, diet composition has been shown to impact sleep, but studies have primarily relied upon varying the concentrations of sugars and protein, or fully food-restricting animals (Catterson et al, 2010; Keene et al, 2010; Linford, Chan, & Pletcher, 2012; Linford, Ro, Chung, & Pletcher, 2015; Yamazaki et al, 2012). Flies have are capable of tasting a number of additional modalities including fatty acids, salt, amino acids, and carbonation (Fischler, Kong, Marella, & Scott, 2007; Masek & Keene, 2013; Toshima & Tanimura, 2012; Zhang, Ni, & Montell, 2013), but the effects of these factors on sleep regulation has not been explored.…”