The tobacco hawkmoth may smell the world not only with its antennae but with its wings.
Sensory bristles along the edges of the moth’s wings respond to two specific volatile amines, and the tissue expresses genes for receptors that could detect them, researchers report in the Journal of Experimental Biology. The findings, they say, show that the wings of Manduca sexta act as accessory olfactory organs that may help the insect choose where to lay its eggs.
Through a combination of advanced imaging techniques, “we revealed that the wings of the hawkmoth M. sexta function as olfactory appendages,” the researchers write in the paper. “We confirmed the presence of sensory bristles on the lateral and posterior margins of the wings.”
Insects are already known to taste and feel with their wings. In fruit flies, wing bristles detect sugars, bitters and cuticular hydrocarbons that guide mating. Genes for odorant, ionotropic and gustatory receptors have also turned up in the wings of beetles, aphids, mosquitoes and moths, raising the possibility that wings can smell airborne chemicals too. Until now, however, no one had tested whether the wings of the tobacco hawkmoth actually respond to odors.
Using scanning electron microscopy, Sonja Bisch-Knaden and colleagues found an average of 21 to 32 short, stout sensory bristles along the margins of each forewing and hindwing. Each bristle sits in a raised socket typical of mechanosensory organs, yet it also carries a pore just below its tip and numerous pores in its wall — features long associated with chemical detection.
Bisch-Knaden et al.
Gene-expression assays revealed transcripts for several ionotropic receptors, including the amine-sensing co-receptor IR76b and two members of a moth-specific clade called IR7d, as well as a handful of odorant-receptor genes. Notably, the obligatory co-receptor ORCo required for most odorant receptors was absent.
When the researchers recorded electrical signals from intact hindwings, only two compounds—pyrrolidine and piperidine—produced clear responses. Both are saturated cyclic amines and chemical building blocks of the alkaloids that accumulate in the solanaceous plants preferred by M. sexta for egg-laying. Structurally related amines, plant headspace collections, and a range of other odorants left the wings silent. Removing the margins did not abolish the responses, implying that additional sensory structures may lie hidden among the dense covering of scales on the wing surface.
Protein-structure predictions and docking simulations pointed to two IR7d receptors as the most likely sensors. In the modeled binding pockets of MsexIR7d.2 and MsexIR7d.3, the same acidic amino acids formed hydrogen bonds with both active amines.
‘This suggests that the moth has special sensory hairs across its wings, not just along the edges, that can smell those odours’, Bisch-Knaden said in a statement.
How wing responses actually shape behavior is still unknown. Sensory neurons from the wing base reach the subesophageal ganglion in the head, a region where many sensory streams converge, but direct tests of wing-driven decisions have not yet been performed. Pyrrolidine alone does not trigger egg-laying in wind-tunnel assays, yet the authors suggest it could still contribute when embedded in the full scent of a host plant, especially if a hovering female scratches the leaf surface with her tarsal spines and releases the compounds.
“Together, these findings demonstrate that the wings of M. sexta function as accessory olfactory organs that may influence oviposition choice,” the authors write. They note that the same amines strongly activate olfactory neurons on the moth’s ovipositor and on a newly described leg organ called the epiphysis, suggesting that non-antennal detection of these compounds is widespread.
Journal Reference: Journal of Experimental Biology. DOI: 10.1242/jeb.252047
