Aniruddha Mitra

It is a challenge to induce an organism to feed on an aversive compound, and this must be overcome to study the noxious effect of ingestion of a bitter compound on the physiology and behavior of the organism. We show that cucurbit[7]uril (CB7) nanoencapsulation significantly reduces the aversive nature of bitter phytochemicals (caffeine and strychnine) in Drosophila melanogaster, and thereby, flies can be induced to feed on phytochemicals that they normally avoid ingesting. This is the first demonstration of CB7-mediated delivery of aversive compounds into insects and can help in the study of the relation between bitterness and toxicity and open up new applications in studying insect physiology and pest control.

Eusocial Hymenoptera colonies are characterized by the presence of altruistic individuals, which rear their siblings instead of their own offspring. In the course of evolution, such sterile castes are thought to have emerged through the process of kin selection, altruistic traits being transmitted to following generation if they benefit relatives. By allowing kinship recognition, the detection of cuticular hydrocarbons (CHCs) might be instrumental for kin selection. In carpenter ants, a female-specific olfactory subsystem processes CHC information through antennal detection by basiconic sensilla. It is still unclear if other families of eusocial Hymenoptera use the same subsystem for sensing CHCs. Here, we examined the existence of such a subsystem in Vespidae (using the hornet Vespa velutina), a family in which eusociality emerged independently of ants. The antennae of both males and female hornets contain large basiconic sensilla. Sensory neurons from the large basiconic sensilla exclusively project to a conspicuous cluster of small glomeruli in the antennal lobe, with anatomical and immunoreactive features that are strikingly similar to those of the ant CHC-sensitive subsystem. Extracellular electrophysiological recordings further show that sensory neurons within hornet basiconic sensilla preferentially respond to CHCs. Although this subsystem is not female-specific in hornets, the observed similarities with the olfactory system of ants are striking. They suggest that the basiconic sensilla subsystem could be an ancestral trait, which may have played a key role in the advent of eusociality in these hymenopteran families by allowing kin recognition and the production of altruistic behaviors toward relatives.

Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, the ligands which activate these neurons define a sensory space called “bitter”. By extension, this term has been used in animals and insects to define molecules which induce aversive responses. In this review, based on our observations carried out in Drosophila, we examine how bitter compounds are detected and if the activation of bitter-sensitive neurons respond only to molecules bitter to humans. Like most animals, flies detect bitter chemicals through a specific population of taste neurons, distinct from those responding to sugars or to other modalities. Activating bitter-sensitive taste neurons induce aversive reactions and inhibits feeding. Bitter molecules also contribute to the suppression of sugar-neuron responses and can lead to a complete inhibition of the responses to sugar at the periphery. Since some bitter molecules activate bitter-sensitive neurons and some inhibit sugar detection, bitter molecules are represented by two sensory spaces which are only partially congruent. In addition to molecules which impact feeding, we recently discovered that the activation of bitter-sensitive neurons also induces grooming. Bitter-sensitive neurons of the wings and of the legs can sense chemicals from the gram negative bacteria, Escherichia coli, thus adding another biological function to these receptors. Bitter-sensitive neurons of the proboscis also respond to inhibitory pheromones such as 7-tricosene. Activating these neurons by bitter molecules in the context of sexual encounter inhibits courting and sexual reproduction, while activating these neurons with 7-tricosene in a feeding context will inhibit feeding. The picture that emerges from these observations is that the taste system is composed of detectors which monitor different “categories” of ligands, which facilitate or inhibit behaviors depending on the context (feeding, sexual reproduction, hygienic behavior), thus considerably extending the initial definition of “bitter” tasting.

In flies and humans, bitter chemicals are known to inhibit sugar detection, but the adaptive role of this inhibition is often overlooked. At best, this inhibition is described as contributing to the rejection of potentially toxic food, but no studies have addressed the relative importance of the direct pathway that involves activating bitter-sensitive cells versus the indirect pathway represented by the inhibition of sugar detection. Using toxins to selectively ablate or inactivate populations of bitter-sensitive cells, we assessed the behavioral responses of flies to sucrose mixed with strychnine (which activates bitter-sensitive cells and inhibits sugar detection) or withl-canavanine (which only activates bitter-sensitive cells). As expected, flies with ablated bitter-sensitive cells failed to detectl-canavanine mixed with sucrose in three different feeding assays (proboscis extension responses, capillary feeding, and two-choice assays). However, such flies were still able to avoid strychnine mixed with sucrose. By means of electrophysiological recordings, we established that bitter molecules differ in their potency to inhibit sucrose detection and that sugar-sensing inhibition affects taste cells on the proboscis and the legs. The optogenetic response of sugar-sensitive cells was not reduced by strychnine, thus suggesting that this inhibition is linked directly to sugar transduction. We postulate that sugar-sensing inhibition represents a mechanism in insects to prevent ingesting harmful substances occurring within mixtures.

Queens in many social insects are known to maintain their status through chemicals (pheromones) and cuticular hydrocarbons and have been the focus of many investigations that have looked at the chemicals involved in queen signaling. In the primitively eusocial wasp Ropalidia marginata Lepeletier (Hymenoptera: Vespidae), the Dufour’s gland has been shown to be involved in queen signaling, and Dufour’s gland hydrocarbons have been found to be correlated with fertility. Hence, this study analyzed the cuticle of R. marginata along with the Dufour’s gland in order to compare their hydrocarbon profiles. The results show that the Dufour’s gland and cuticle contained the same set of hydrocarbons in similar proportions (for the majority of compounds). Patterns pertaining to fertility signaling present in cuticular hydrocarbons were also similar to those present in the Dufour’s gland hydrocarbons. Furthermore, the haemolymph contained the same hydrocarbons as found in the Dufour’s gland and cuticle in similar proportions, thereby providing an explanation as to why the hydrocarbon profiles of the Dufour’s gland and cuticle are correlated.