Immediate and delayed effects of nutrient-sensing in fruit fly Drosophila melanogaster

Abstract

Starting in late 1980’s, Bill Timberlake and associates conducted a series of experiments on anticipatory contrast which showed that rats’ feeding decisions were regulated by the nutritive value of currently ingested and anticipated food. The effects of nutrient sensing on feeding regulation have been studied intensively in rodents, and recently, in the fruit fly Drosophila melanogaster. In this study, we developed a new behavioral test to study rapid feeding decisions of tethered flies within 6–8 s of ingestion. Using a two-phase experimental design, we presented individual flies one of four serial combinations of a non-nutritive sugar, arabinose, or a nutritive sugar, sucrose. Feeding decisions of wildtype (Canton-S) flies are altered both by immediate effects of nutrient sensing and 1-hour delayed effects of nutrient-feeding, and the two effects act additively to yield a signature pattern of behavioral contrast based on nutritive contrast. Feeding phenotype of flies that carry a mutation of the dSLC5A11 (cupcake) gene varied with the mutant allele and genetic background. Fasted dSLC5A11 mutants showed an overeating phenotype and a defect in short-term feeding regulation irrespective of the nutritive value of sugar. Flies that carried the dSLC5A111 allele showed differential feeding for arabinose and sucrose. However, dSLC5A112 allele yielded a conspicuous deficit in delayed effects of nutrient ingestion, but only when it was expressed on a Canton-S background. Our results suggest that dSLC5A11 might function to integrate external stimulus properties and internal state for feeding regulation and action selection.