Chemoreception is essential for survival. Feeding, mating, and avoidance of predators depend on detection of sensory cues. Drosophila contains diverse families of chemoreceptors that detect odors, tastants, pheromones, and noxious stimuli, including receptors of the Or, Gr, IR, Ppk, and Trp families. We consider recent progress in understanding chemoreception in the fly, including the identification of new receptors, the discovery of novel biological functions for receptors, and the localization of receptors in unexpected places. We discuss major unsolved problems and suggest areas that may be particularly ripe for future discoveries, including the roles of these receptors in driving the circuits and behaviors that are essential to the survival and reproduction of the animal.

Selection of appropriate oviposition sites is essential for progeny survival and fitness in generalist insect species, such as Drosphila melanogaster, yet little is known about the mechanisms regulating how environmental conditions and innate adult preferences are evaluated and balanced to yield the final substrate choice for eggdeposition. Female D. melanogaster are attracted to food containing acetic acid (AA) as an oviposition substrate. However, our observations reveal that this egg-laying preference is a complex process, as it directly opposes an otherwise strong, default behavior of positional avoidance for the same food. We show that 2 distinct sensory modalities detect AA. Attraction to AA-containing food for the purpose of egg-laying relies on the gustatory system, while positional repulsion depends primarily on the olfactory system. Similarly, distinct central brain regions are involved in AA attraction and repulsion. Given this unique situation, in which a single environmental stimulus yields 2 opposing behavioral outputs, we propose that the interaction of egg-laying attraction and positional aversion for AA provides a powerful model for studying how organisms balance competing behavioral drives and integrate signals involved in choice-like processes.choice behavior ͉ gustatory system ͉ olfactory system ͉ mushroom body ͉ ellipsoid body O viposition provides a powerful yet simple means for monitoring preference behavior in Drosophila melanogaster, since a laid egg represents a marker for female position. Past studies have used egg laying as a readout for conditions advantageous to progeny development (1, 2), in which oviposition preference effectively separates larvae of different sibling species of Drosophila. Egg laying has also been used to detect aversion toward compounds toxic to both larvae and adults (3, 4). Furthermore, numerous studies have used patterns of oviposition to distinguish subtle differences in host plant preferences, which have provided insights into resource requirements and ecological behaviors of different Drosophila species (5, 6).Despite numerous studies using oviposition-site selection as a behavioral readout, direct study of the relevant sensory circuits and the oviposition program itself have been initiated only recently in D. melanogaster (7,8). To investigate the genetic mechanisms and neural circuits regulating this important behavioral choice in D. melanogaster, we developed a simple yet robust 2-choice assay that utilizes acetic acid (AA), a naturally occurring product of fruit fermentation, as an egg-laying attractant (9, 10). However, in addition to verifying a strong egg-laying preference for AA, we surprisingly observed D. melanogaster show a strong positional aversion to the same AA-containing food. We demonstrate that when sampling for oviposition sites, females integrate input from distinct sensory modalities to choose a particular behavioral output from 2 competing options: ovipositional attraction for and positional repulsion to AA. Egg-laying preference is p...

The neural control of sugar consumption is critical for normal metabolism. In contrast to sugar-sensing taste neurons that promote consumption, we identify a taste neuron that limits sucrose consumption in Drosophila. Silencing of the neuron increases sucrose feeding; optogenetic activation decreases it. The feeding inhibition depends on the IR60b receptor, as shown by behavioral analysis and Ca2+ imaging of an IR60b mutant. The IR60b phenotype shows a high degree of chemical specificity when tested with a broad panel of tastants. An automated analysis of feeding behavior in freely moving flies shows that IR60b limits the duration of individual feeding bouts. This receptor and neuron provide the molecular and cellular underpinnings of a new element in the circuit logic of feeding regulation. We propose a dynamic model in which sucrose acts via IR60b to activate a circuit that inhibits feeding and prevents overconsumption.DOI: http://dx.doi.org/10.7554/eLife.24992.001

Understanding sensory systems that perceive environmental inputs and neural circuits that select appropriate motor outputs is essential for studying how organisms modulate behavior and make decisions necessary for survival. Drosophila melanogaster oviposition is one such important behavior, in which females evaluate their environment and choose to lay eggs on substrates they may find aversive in other contexts. We employed neurogenetic techniques to characterize neurons that influence the choice between repulsive positional and attractive egg-laying responses toward the bitter-tasting compound lobeline. Surprisingly, we found that neurons expressing Gr66a, a gustatory receptor normally involved in avoidance behaviors, receive input for both attractive and aversive preferences. We hypothesized that these opposing responses may result from activation of distinct Gr66a-expressing neurons. Using tissue-specific rescue experiments, we found that Gr66a-expressing neurons on the legs mediate positional aversion. In contrast, pharyngeal taste cells mediate the egg-laying attraction to lobeline, as determined by analysis of mosaic flies in which subsets of Gr66a neurons were silenced. Finally, inactivating mushroom body neurons disrupted both aversive and attractive responses, suggesting that this brain structure is a candidate integration center for decision-making during Drosophila oviposition. We thus define sensory and central neurons critical to the process by which flies decide where to lay an egg. Furthermore, our findings provide insights into the complex nature of gustatory perception in Drosophila. We show that tissue-specific activation of bitter-sensing Gr66a neurons provides one mechanism by which the gustatory system differentially encodes aversive and attractive responses, allowing the female fly to modulate her behavior in a context-dependent manner.

SUMMARY Taste drives appropriate food preference and intake. In Drosophila, taste neurons are housed in both external and internal organs, but the latter have been relatively underexplored. Here, we report that Poxn mutants with a minimal taste system of pharyngeal neurons can avoid many aversive tastants, including bitter compounds, acid, and salt, suggesting that pharyngeal taste is sufficient for rejecting intake of aversive compounds. Optogenetic activation of selected pharyngeal bitter neurons during feeding events elicits changes in feeding parameters that can suppress intake. Functional dissection experiments indicate that multiple classes of pharyngeal neurons are involved in achieving behavioral avoidance, by virtue of being inhibited or activated by aversive tastants. Tracing second-order pharyngeal circuits reveals two main relay centers for processing pharyngeal taste inputs. Together, our results suggest that the pharynx can control the ingestion of harmful compounds by integrating taste input from different classes of pharyngeal neurons.