The pleiotropic effects of Innexin genes expressed in Drosophila glia encompass wing chemosensory sensilla.

The neuroanatomy of Drosophila wing chemosensilla and the analysis of their sensory organ precursor cell lineage have demonstrated that they are surprisingly related to taste perception. The microarchitecture of wing bristles limits the use of electrophysiology methods to investigate wing chemosensory mechanisms. However, by monitoring the fluorescence of the complex calcium/GCaMP, calcium flux triggered upon tastant stimulation was observed within sensilla aligned along the wing anterior nerve. This string of fluorescent puncta was impaired in wings of Innexin 2 (Inx2) mutant flies; although it is unclear whether the Innexin proteins act at the level of the wing imaginal disc, adult wing and/or at both levels. Glial cells known to shelter Innexin(s) expression have no documented role in adult chemosensory sensilla. Our data suggest that Innexin(s) are likely required for the maturation of functional wing chemosensilla in adulthood. The unexpected presence of most Innexin transcripts in adult wing RNAseq data set argues for the expression of Innexin proteins in the larval imaginal wing disc that are continued in wing chemosensilla at adulthood. OPEN PRACTICES: This article has earned an Open Data badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available as supporting materials and includes the electronic lab notebook. Learn more about the Open Practices badges from the Center for Open Science: https://osf.io/tvyxz/wiki.

Functional Gustatory Role of Chemoreceptors in Drosophila Wings.

Neuroanatomical evidence argues for the presence of taste sensilla in Drosophila wings; however, the taste physiology of insect wings remains hypothetical, and a comprehensive link to mechanical functions, such as flight, wing flapping, and grooming, is lacking. Our data show that the sensilla of the Drosophila anterior wing margin respond to both sweet and bitter molecules through an increase in cytosolic Ca(2+) levels. Conversely, genetically modified flies presenting a wing-specific reduction in chemosensory cells show severe defects in both wing taste signaling and the exploratory guidance associated with chemodetection. In Drosophila, the chemodetection machinery includes mechanical grooming, which facilitates the contact between tastants and wing chemoreceptors, and the vibrations of flapping wings that nebulize volatile molecules as carboxylic acids. Together, these data demonstrate that the Drosophila wing chemosensory sensilla are a functional taste organ and that they may have a role in the exploration of ecological niches.

Nano-architecture of gustatory chemosensory bristles and trachea in Drosophila wings.

In the Drosophila wing anterior margin, the dendrites of gustatory neurons occupy the interior of thin and long bristles that present tiny pores at their extremities. Many attempts to measure ligand-evoked currents in insect wing gustatory neurons have been unsuccessful for technical reasons. The functions of this gustatory activity therefore remain elusive and controversial. To advance our knowledge on this understudied tissue, we investigated the architecture of the wing chemosensory bristles and wing trachea using Raman spectroscopy and fluorescence microscopy. We hypothesized that the wing gustatory hair, an open-ended capillary tube, and the wing trachea constitute biological systems similar to nano-porous materials. We present evidence that argues in favour of the existence of a layer or a bubble of air beneath the pore inside the gustatory hair. We demonstrate that these hollow hairs and wing tracheal tubes fulfil conditions for which the physics of fluids applied to open-ended capillaries and porous materials are relevant. We also document that the wing gustatory hair and tracheal architectures are capable of trapping volatile molecules from the environment, which might increase the efficiency of their spatial detection by way of wing vibrations or during flight.

Trade-off between toxicity and signal detection orchestrated by frequency- and density-dependent genes.

Behaviors in insects are partly highly efficient Bayesian processes that fulfill exploratory tasks ending with the colonization of new ecological niches. The foraging (for) gene in Drosophila encodes a cGMP-dependent protein kinase (PKG). It has been extensively described as a frequency-dependent gene and its transcripts are differentially expressed between individuals, reflecting the population density context. Some for transcripts, when expressed in a population at high density for many generations, concomitantly trigger strong dispersive behavior associated with foraging activity. Moreover, genotype-by-environment interaction (GEI) analysis has highlighted a dormant role of for in energetic metabolism in a food deprivation context. In our current report, we show that alleles of for encoding different cGMP-dependent kinase isoforms influence the oxidation of aldehyde groups of aromatic molecules emitted by plants via Aldh-III and a phosphorylatable adaptor. The enhanced efficiency of oxidation of aldehyde odorants into carboxyl groups by the action of for lessens their action and toxicity, which should facilitate exploration and guidance in a complex odor environment. Our present data provide evidence that optimal foraging performance requires the fast metabolism of volatile compounds emitted by plants to avoid neurosensory saturation and that the frequency-dependent genes that trigger dispersion influence these processes.