Non-Canonical Odor Coding in the Mosquito

Abstract

Female Aedes aegypti mosquitoes show strong innate attraction to humans. This chemosensory behavior is critical to species survival because females require a blood-meal to reproduce. Humans, the preferred host of Ae. aegypti, produce a complex blend of odor cues along with carbon dioxide (CO2) that attracts females ready to bite. Mosquitoes detect these cues with heteromeric ligand-gated ion channels encoded by three different chemosensory receptor gene families. A common theme in other species is that olfactory neurons express a single receptor that defines their chemical specificity and that they extend axons that converge upon dedicated glomeruli in the first sensory processing center in the brain. Such an organization permits the brain to segregate olfactory information and monitor activity of individual glomeruli to interpret what smell has been encountered. We have discovered that Ae. aegypti uses an entirely different organizational principle for its olfactory system. Using genetic strains that label subpopulations of olfactory neurons, we found that many neurons co-express multiple members of at least two of the chemosensory receptor families. This unexpected co-expression is functional, as assessed by in vivo calcium imaging showing that a given glomerulus is activated by multiple ligands detected by different receptor families. This has direct functional consequences for mosquito behavior. Mutant mosquitoes that cannot sense CO2 can be behaviorally activated by a volatile amine that stimulates the CO2 glomerulus. This non-canonical olfactory system organization featuring overlapping receptor expression may explain the female mosquito's robust and unbreakable attraction to humans.

Single-cell transcriptomes of developing and adult olfactory receptor neurons in Drosophila

“…The extent of co-expression of these co-receptors may be underestimated due to dropouts or expression below our stringent threshold. Our findings are in line with two recent studies that reveal broad expression and function of Ir and Or co-receptors in Drosophila and mosquitos ( Task et al, 2020 ; Younger et al, 2020 ).…”

Chemoreceptor Co-Expression inDrosophilaOlfactory Neurons

“…The work presented here raises the possibility that other insects may also exhibit polymodal expression of chemosensory receptors. Exciting new work in Aedes aegypti mosquitoes suggests that this may indeed be the case: mosquito olfactory neurons can co-express Orco/IrCo/Gr receptors; in the CO 2 -sensing olfactory neuron, this polymodal co-expression functionally expands the range of activating odors (Younger, Herre et al, 2020). This suggests that polymodal expression of chemosensory receptors may be an important feature of insect olfactory neurons.…”

Activity and stress during a critical period regulate olfactory sensory neuron differentiation

“…But when the environment changes, inducing stress, the expression of the dormant OR alleles or paralogues can be activated leading to individualization of the OR expression and the odor responses in the population. Interestingly, the OSNs that express ORs also express IR co-receptors in both Drosophila and mosquitoes (Task et al, 2020; Younger et al, 2020), suggesting that ORs and IRs are co-expressed in some OSN classes. Electrophysiology also shown that some OSN classes in Drosophila (Ab1b, Ab3a and Ab6a) respond to IR odors (de Bruyne et al, 2001), suggesting that stress can tweak the balance between co-expressed ORs and IRs.…”