A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila.

Flies, like all animals, need to find suitable and safe food. Because the principal food source for Drosophila melanogaster is yeast growing on fermenting fruit, flies need to distinguish fruit with safe yeast from yeast covered with toxic microbes. We identify a functionally segregated olfactory circuit in flies that is activated exclusively by geosmin. This microbial odorant constitutes an ecologically relevant stimulus that alerts flies to the presence of harmful microbes. Geosmin activates only a single class of sensory neurons expressing the olfactory receptor Or56a. These neurons target the DA2 glomerulus and connect to projection neurons that respond exclusively to geosmin. Activation of DA2 is sufficient and necessary for aversion, overrides input from other olfactory pathways, and inhibits positive chemotaxis, oviposition, and feeding. The geosmin detection system is a conserved feature in the genus Drosophila that provides flies with a sensitive, specific means of identifying unsuitable feeding and breeding sites.

Host plant-driven sensory specialization in Drosophila erecta.

Finding appropriate feeding and breeding sites is crucial for all insects. To fulfil this vital task, many insects rely on their sense of smell. Alterations in the habitat--or in lifestyle--should accordingly also be reflected in the olfactory system. Solid functional evidence for direct adaptations in the olfactory system is however scarce. We have, therefore, examined the sense of smell of Drosophila erecta, a close relative of Drosophila melanogaster and specialist on screw pine fruits (Pandanus spp.). In comparison with three sympatric sibling species, D. erecta shows specific alterations in its olfactory system towards detection and processing of a characteristic Pandanus volatile (3-methyl-2-butenyl acetate, 3M2BA). We show that D. erecta is more sensitive towards this substance, and that the increased sensitivity derives from a numerical increase of one olfactory sensory neuron (OSN) class. We also show that axons from these OSNs form a complex of enlarged glomeruli in the antennal lobe, the first olfactory brain centre, of D. erecta. Finally, we show that 3M2BA induces oviposition in D. erecta, but not in D. melanogaster. The presumed adaptations observed here follow to a remarkable degree those found in Drosophila sechellia, a specialist upon noni fruit, and suggest a general principle for how specialization affects the sense of smell.

Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster.

As a model for primary olfactory perception, the antennal lobe (AL) of Drosophila melanogaster is among the most thoroughly investigated and well-understood neuronal structures. Most studies investigating the functional properties and neuronal wiring of the AL are conducted in vivo, although so far the AL morphology has been mainly analyzed in vitro. Identifying the morphological subunits of the AL-the olfactory glomeruli-is usually done using in vitro AL atlases. However, the dissection and fixation procedure causes not only strong volumetric but also geometrical modifications; the result is unpredictable dislocation and a distortion of the AL glomeruli between the in vitro and in vivo brains. Hence, to characterize these artifacts, which are caused by in vitro processing, and to reliably identify glomeruli for in vivo applications, we generated a transgenic fly that expresses the red fluorescent protein DsRed directly fused to the presynaptic protein n-synaptobrevin, under the control of the pan-neuronal promotor elav to label the neuropil in the live animal. Using this fly line, we generated a digital 3D atlas of the live Drosophila AL; this atlas, the first of its kind, provides an excellent geometric match for in vivo studies. We verified the identity of 63% of AL glomeruli by mapping the projections of 34 GAL4-lines of individual chemosensory receptor genes. Moreover, we characterized the innervation patterns of the two most frequently used GAL4-lines in olfactory research: Orco- and GH146-GAL4. The new in vivo AL atlas will be accessible online to the neuroscience community.

Decoding odor quality and intensity in the Drosophila brain.

To internally reflect the sensory environment, animals create neural maps encoding the external stimulus space. From that primary neural code relevant information has to be extracted for accurate navigation. We analyzed how different odor features such as hedonic valence and intensity are functionally integrated in the lateral horn (LH) of the vinegar fly, Drosophila melanogaster. We characterized an olfactory-processing pathway, comprised of inhibitory projection neurons (iPNs) that target the LH exclusively, at morphological, functional and behavioral levels. We demonstrate that iPNs are subdivided into two morphological groups encoding positive hedonic valence or intensity information and conveying these features into separate domains in the LH. Silencing iPNs severely diminished flies' attraction behavior. Moreover, functional imaging disclosed a LH region tuned to repulsive odors comprised exclusively of third-order neurons. We provide evidence for a feature-based map in the LH, and elucidate its role as the center for integrating behaviorally relevant olfactory information.

Spatial representation of odorant valence in an insect brain.

Brains have to decide whether and how to respond to detected stimuli based on complex sensory input. The vinegar fly Drosophila melanogaster evaluates food sources based on olfactory cues. Here, we performed a behavioral screen using the vinegar fly and established the innate valence of 110 odorants. Our analysis of neuronal activation patterns evoked by attractive and aversive odorants suggests that even though the identity of odorants is coded by the set of activated receptors, the main representation of odorant valence is formed at the output level of the antennal lobe. The topographic clustering within the antennal lobe of valence-specific output neurons resembles a corresponding domain in the olfactory bulb of mice. The basal anatomical structure of the olfactory circuit between insects and vertebrates is known to be similar; our study suggests that the representation of odorant valence is as well.

A deceptive pollination system targeting drosophilids through olfactory mimicry of yeast.

In deceptive pollination, insects are bamboozled into performing nonrewarded pollination. A prerequisite for the evolutionary stability in such systems is that the plants manage to generate a perfect sensory impression of a desirable object in the insect nervous system [1]. The study of these plants can provide important insights into sensory preference of their visiting insects. Here, we present the first description of a deceptive pollination system that specifically targets drosophilid flies. We show that the examined plant (Arum palaestinum) accomplishes its deception through olfactory mimicry of fermentation, a strategy that represents a novel pollination syndrome. The lily odor is composed of volatiles characteristic of yeast, and produces in Drosophila melanogaster an antennal detection pattern similar to that elicited by a range of fermentation products. By functional imaging, we show that the lily odors target a specific subset of odorant receptors (ORs), which include the most conserved OR genes in the drosophilid olfactome. Furthermore, seven of eight visiting drosophilid species show a congruent olfactory response pattern to the lily, in spite of comprising species pairs separated by ∼40 million years [2], showing that the lily targets a basal function of the fly nose, shared by species with similar ecological preference.