Aniruddha Mitra | Centre National de la Recherche Scientifique / French National Centre for Scientific Research (original) (raw)

Papers by Aniruddha Mitra

Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, ... more 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 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 induces 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 the inhibitory pheromone, 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.

Sex pheromones are vital in communication between individuals belonging to opposite sexes and for... more Sex pheromones are vital in communication
between individuals belonging to opposite sexes and form
an integral part of the reproductive biology of various spe-
cies. Among insects, sexual dimorphism in CHCs has been
reported from diverse taxa spanning seven different orders,
and thereby CHCs have been implicated as sex pheromones.
Because males and females of the primitively eusocial wasp
Ropalidia marginata touch each other with their antennae
during mating, before engaging in sperm transfer, a sex
pheromone that is perceived via contact chemosensation
through the antennae can possibly exist in this species. Since
CHCs have been implied as sex pheromones in various in-
sects (including hymenopterans), and since sexual
dimorphism of CHCs should be an obligatory prerequisite
for them to act as sex pheromones, we investigated whether
males and females of R. marginata differ in their CHC profiles. We found only nonvolatile CHCs, and our results
show absence of sexual dimorphism in CHCs, suggesting
that CHCs do not function as sex pheromone in this species.
A behavioral assay failed to show presence of mate attrac-
tion at a distance, thereby showing the absence of volatile
long-distance mate attraction cues (that may originate from
sources other than and in addition to CHCs).

In flies and humans, bitter chemicals are known to inhibit sugar detection, but the adaptive role... more 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 with L-canavanine (which only activates bitter-sensitive cells). As expected, flies with ablated bitter-sensitive cells failed to detect L-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.

Ropalidia marginata is a primitively eusocial (truly social) wasp found in peninsular India. It i... more Ropalidia marginata is a primitively eusocial (truly social) wasp found in peninsular India. It is different from the typical
primitively eusocial species in having docile queens that cannot use aggression to maintain reproductive monopoly. Recent
studies using chemical analysis and bioassays indicate that Dufour’s gland is a source of the queen pheromone in this
species. Queens appear to signal their presence to workers through their Dufour’s gland compounds, possibly by applying
them on the nest surface, and this results in suppression of reproduction by workers, resulting in reproductive monopoly
by the queen. The Dufour’s gland was found to contain saturated long chain hydrocarbons, which have recently been
suggested to be the ancestral state of fertility signals in Hymenoptera. The Dufour’s gland composition differed significantly between queens and workers, and was also correlated with the state of ovarian development, varying continuously as a function of ovarian development, thereby advocating the honesty of the queen pheromone. This elucidates the mechanism of maintenance of eusociality through pheromonal queen signalling by the Dufour’s gland compounds.

"Nestmate discrimination plays an important role in preserving the integrity of social insect col... more "Nestmate discrimination plays an important role in preserving the integrity of social insect colonies. It is
known to occur in the primitively eusocial wasp Ropalidia marginata in which non-nestmate conspecifics
are not allowed to come near a nest. However, newly eclosed females are accepted in foreign colonies,
suggesting that such individuals may not express the cues that permit differentiation between nestmates
and non-nestmates. As cuticular hydrocarbons (CHCs) have been implicated as chemosensory cues used
in nestmate recognition in other species, we investigated, using bioassays and chemical analyses,
whether CHCs can play a role in nestmate recognition in R. marginata. We found that individuals can be
differentiated according to colony membership using their CHC profiles, suggesting a role of CHCs in
nestmate discrimination. Non-nestmate CHCs of adult females received more aggression than nestmate
CHCs, thereby showing that CHCs are used as cues for nestmate recognition. Contrarily, and as expected,
CHCs of newly eclosed females were not discriminated against when presented to a foreign colony.
Behavioural sequence analysis revealed the behavioural mechanism involved in sensing nestmate
recognition cues.We also found that newly eclosed females had a different CHC profile from that of adult
females, thereby providing an explanation for why young females are accepted in foreign colonies."

"The poison gland and Dufour’s gland are the two glands associated with the sting apparatus in fe... more "The poison gland and Dufour’s gland are the two glands associated with the sting apparatus in female
Apocrita (Hymenoptera). While the poison gland usually functions as an integral part of the venom delivery
system, the Dufour’s gland has been found to differ in its function in various hymenopteran groups.
Like all exocrine glands, the function of the Dufour’s gland is to secrete chemicals, but the nature and
function of the secretions varies in different taxa. Functions of the Dufour’s gland secretions range from
serving as a component of material used in nest building, larval food, and pheromones involved in communicative
functions that are important for both solitary and social species. This review summarizes the
different functions reported for the Dufour’s gland in hymenopterans, illustrating how the Dufour’s gland
secretions can be adapted to give rise to various functions in response to different challenges posed by the
ways of life followed by different taxa. Aspects of development, structure, chemistry and the evolution of
different functions are also touched upon briefly."

Journal of Insect Science

Queens in many social insects are known to maintain their status through chemicals (pheromones) a... more 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.

Current Science, Apr 2013

"Metamorphosis in insects is a remarkable phenomenon where the larva undergoes a striking morphol... more "Metamorphosis in insects is a remarkable phenomenon where the larva undergoes a striking morphological reorganization to give rise to the adult. Over the
years, various physiological factors and pathways that
govern metamorphosis have been discovered, and at
the same time, some understanding about the origins
of this phenomenon has also emerged. This review
summarizes the current state of knowledge of both the
mechanisms underlying metamorphosis, as well as the
theories put forward to explain its evolution.
"

This thesis has looked at the proximate mechanisms by which eusociality is maintained in colonies... more This thesis has looked at the proximate mechanisms by which eusociality is maintained in colonies of the primitively eusocial wasp Ropalidia marginata. Unlike other typical primitively eusocial species, the R, marginata queen is remarkably docile and non-interactive and hence cannot possibly use aggression to maintain her status. Recent evidence hints at pheromonal queen signalling through the Dufour's gland. Hence, queen-worker difference in Dufour's gland composition has been studied in details.

Ethology, 2012

Ropalidia marginata, a primitively eusocial wasp, is different from typical primitively eusocial ... more Ropalidia marginata, a primitively eusocial wasp, is different from typical primitively eusocial species in having docile queens who cannot be using dominance to maintain reproductive monopoly and instead appear to use a pheromone from the Dufour's gland to do so. When a docile queen is removed from her colony, one of the workers (potential queen, PQ) becomes highly aggressive, and if the queen is not returned, gradually loses her aggression and becomes the new docile queen within a few days. We hypothesized that the decrease in aggression of the PQ with time since queen removal should be correlated with her change in ovaries and pheromone profile. Because the Dufour's gland hydrocarbon composition in R. marginata can be correlated with fertility, this also gave us an opportunity to test whether PQ is different from workers in her Dufour's gland hydrocarbons. In this study, we therefore trace the road to royalty in R. marginata, that is, the transition of the PQ during queen establishment, in terms of her ovaries, aggression, and Dufour's gland hydrocarbons. Our study focuses on queen establishment, which is important for understanding how reproductive conflict can be manifested and resolved.

Sociobiology , 2012

""Ropalidia marginata is a primitively eusocial paper wasp found in peninsular India, where rece... more ""Ropalidia marginata is a primitively eusocial paper wasp found in peninsular
India, where recent work suggests the role of the Dufour’s gland hydrocarbons in queen signaling. It appears that the queen signals her presence to workers by rubbing the tip of her abdomen on the nest surface, thereby presumably applying her Dufour’s gland secretion to the nest. Since the queen alone produces pheromone from the Dufour’s gland and also applies it on the nest surface, the activity level of queen gland should be higher than that of worker gland, as the gland contents would have to get replenished periodically for queens but not for workers. The difference in activity level can be manifested in difference in Dufour’s gland morphology, larger glands implying higher activity levels and smaller glands implying lower activity levels, as positive correlation between gland size and gland activity has been reported in exocrine glands of various taxa (including Hymenopteran insects). Hence we investigated whether there is any size difference between Dufour’s glands of queens and workers in R. marginata. We found that there was no difference between queens and workers in their Dufour’s gland size, implying that Dufour’s gland activity and Dufour’s gland size are likely to be uncorrelated in this species.
""

Queens of many social insect species are known to maintain reproductive monopoly by pheromonal si... more Queens of many social insect species are known to maintain reproductive monopoly by pheromonal signalling of fecundity. Queens of the primitively eusocial wasp Ropalidia marginata appear to do so using secretions from their Dufour’s glands, whose hydrocarbon composition is correlated with fertility. Solitary nest foundresses of R. marginata are without nestmates; hence expressing a queen signal can be redundant, since there is no one to receive the signal. But if queen pheromone is an honest signal inextricably linked with fertility, it should correlate with fertility and be expressed irrespective of the presence or absence of receivers of the signal, by virtue of being a byproduct of the state of fertility. Hence we compared the Dufour’s gland hydrocarbons and ovaries of solitary foundresses with queens and workers of post-emergence nests. Our results suggest that queen pheromone composition in R. marginata is a byproduct of fertility and hence can honestly signal fertility. This provides important new evidence for the honest signalling hypothesis.

Unlike queens of typical primitively eusocial species, Ropalidia marginata queens are docile and ... more Unlike queens of typical primitively eusocial species, Ropalidia marginata queens are docile and non-interactive, and hence cannot be using dominance to maintain their status. It appears that the queen maintains reproductive monopoly through a pheromone, of which the Dufour’s gland is at least one source. Here we reconfirm earlier results showing that queens and workers can be correctly classified on a discriminant function using the compositions of their respective Dufour’s glands, and also demonstrate consistent queen-worker differences based on categories of compounds and on single compounds also in some cases. Since the queen pheromone is expected to be an honest signal of the fecundity of a queen, we investigate the correlation of Dufour’s gland compounds with ovarian activation of queens. Our study shows that Dufour’s gland compounds in R. marginata correlate with the state of ovarian activation of queens, suggesting that such compounds may portray the fecundity of a queen, and may indeed function as honest signals of fertility.

Queens of the primitively eusocial wasp Ropalidia marginata appear to maintain reproductive monop... more Queens of the primitively eusocial wasp Ropalidia marginata appear to maintain reproductive monopoly through pheromone rather than through physical aggression. Upon queen removal, one of the workers (potential queen, PQ) becomes extremely aggressive but drops her aggression immediately upon returning the queen. If the queen is not returned, the PQ gradually drops her aggression and becomes the next queen of the colony. In a previous study, the Dufour’s gland was found to be at least one source of the queen pheromone. Queen-worker classification could be done with 100% accuracy in a discriminant analysis, using the compositions of their respective Dufour’s glands. In a bioassay, the PQ dropped her aggression in response to the queen’s Dufour’s gland macerate, suggesting that the queen’s Dufour’sgland contents mimicked the queen herself. In the present study, we found that the PQ also dropped her aggression in response to the macerate of a foreign queen’s Dufour’s gland. This suggests that the queen signal is perceived across colonies. This also suggests that the Dufour’s gland in R. marginata does not contain information about nestmateship, because queens are attacked when introduced into foreign
colonies, and hence PQ is not expected to reduce her aggression in response to a foreign queen’s signal.The latter conclusion is especially significant because the Dufour’s gland chemicals are adequate to classify individuals correctly not only on the basis of fertility status (queen versus worker) but also
according to their colony membership, using discriminant analysis. This leads to the additional conclusion (and precaution) that the ability to statistically discriminate organisms using their chemical profiles does not necessarily imply that the organisms themselves can make such discrimination.

As expected for a primitively eusocial wasp, queens and workers are not morphologically different... more As expected for a primitively eusocial wasp, queens and workers are not morphologically differentiated in Ropalidia marginata. As unexpected for a primitively eusocial wasp however, R. marginata queens are remarkably meek and docile. Upon removal of the queen, one of the workers becomes extremely aggressive but immediately drops her aggression if the queen is returned. If the queen is not returned, this hyper-aggressive individual will develop her ovaries, lose almost all her aggression, and become the next queen of the colony. Hence we call her the potential queen (PQ). Because of the non-aggressive nature of the queen and because the PQ loses her aggression by the time she starts laying eggs, we consider the hypothesis that regulation of worker reproduction in R. marginata is mediated by pheromones rather than by physical aggression. Using the immediate loss of aggression by the PQ upon return of the queen, we develop a bioassay to demonstrate that the queen’s Dufour’s gland is at least one of the sources of the queen pheromone. Extracts of the queen’s Dufour’s gland (but not that of the worker’s Dufour’s gland) mimic the queen in making the PQ drop her aggression. We are also able to correctly classify queens and workers by a discriminant function analysis based on the chemical compositions of their respective Dufour’s glands.

Talks by Aniruddha Mitra

Manganese (Mn2+) is an essential transition metal involved in growth, development, cellular respi... more Manganese (Mn2+) is an essential transition metal involved in growth, development, cellular respiration and energy homeostasis, acting as a cofactor for various enzymes. Maintaining homeostatic balance of divalent metal ions like Mn2+ is critical for physiology. Mn2+ transporter proteins have been found to be involved in taste behavior in insects. Thus developing a proper understanding of the role of Mn2+ in modulating sensory systems (e.g., taste) will help in elucidating its role in modulating behavior. The fruit fly Drosophila melanogaster was used as a model to study the effect of Mn2+ on the nervous system. Preliminary results showed that flies raised from egg to adult in food that contains Mn2+ have higher levels of the biogenic amines Dopamine (DA) and Octopamine (OA) but not Serotonin (5-HT) in their brains, as compared to control flies. Since both DA and OA are known to be involved in regulating various behaviors, we hypothesized that the effects of disruptions in Mn2+ homeostasis on behavior are mediated by a direct impact on aminergic signaling in the insect brain. We followed up on these results by raising flies in different concentrations of Mn2+, followed by determination of brain amine levels, aminergic neuroanatomy, gene transcription, and behavioral outcomes. Evidence was found suggesting that Mn2+ may affect biogenic amine levels by impacting transcription levels of genes involved in biogenic amine synthesis pathways, and it was also found that Mn2+ treatment can affect gustatory behavior, whereas aminergic neuroanatomy remains unaffected on exposure to Mn2+ levels that change behavior and aminergic gene expression.

Journal of Insect Science

Current Science, Apr 2013

Ethology, 2012

Sociobiology , 2012