Abstract

Olfactory systems evolved to detect and identify volatile chemical cues, in many cases across great distances. However, the precision of copulatory and oviposition behaviors suggest that they may be guided by olfactory cues detected by sensory systems located on or near the ovipositor. Here we present evidence of a small number of functional olfactory sensilla on the ovipositor of the hawkmoth Manduca sexta. Gene expression analysis of isolated ovipositor tissue indicated active transcription of gustatory and both classes of olfactory receptor genes. Expression of the olfactory co-receptor ORCo and the antennal ionotropic co-receptors IR8a and IR25a suggests that functional olfactory proteins may be present in the sensory structures located on the ovipositor. Scanning electron microscopy identified five to nine porous sensilla on each of the anal papillae of the ovipositor. Furthermore, HRP immunostaining indicated that these sensilla are innervated by the dendrite-like structures from multiple neurons. Finally, we functionally characterized neural responses in these sensilla using single sensillum recordings. Stimulation with a panel of 142 monomolecular odorants revealed that these sensilla indeed house functional olfactory sensory neurons (OSNs). While it remains to be determined what role these chemosensory sensilla play in odor and gustatory guided behaviors, our data clearly demonstrate an olfactory function for neurons present in M. sexta ovipositor sensilla.

Highlights

  • Among the most important sensory abilities of winged insects is the ability to detect, identify and locate the sources of relevant volatile chemical cues

  • The reads were trimmed for both adaptor sequences and quality, and mapped against a reference that was based on the available official gene set (OGS2.0, Kanost et al, 2016), with replaced chemosensory receptor gene models as described in Koenig et al (2015)

  • Our results demonstrate that a small number of sensory sensilla located on the ovipositor of the tobacco hornworm M. sexta possess cells that function as olfactory sensory neurons (OSNs)

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Summary

Introduction

Among the most important sensory abilities of winged insects is the ability to detect, identify and locate the sources of relevant volatile chemical cues. Odorants are primarily detected by olfactory sensory neurons (OSNs) situated on the antennae and, to a lesser extend, the maxillary palps (Wicher, 2015) The dendrites of these OSNs stretch into porous hair-like structures, the olfactory sensilla. It is the chemically-sensitive receptor in the dendritic membrane of these sensory cells that mediate the neural response to odorants (Wicher, 2015). The unrelated antennal IRs were more recently identified as odorant detecting (Benton et al, 2009); they likely form heteromeric complexes with either of two IR co-receptors, IR8a or IR25a and variable IR partners (Abuin et al, 2011; Rytz et al, 2013). Such IRs are involved in the detection of other sensory stimuli, like tastants and sound (Senthilan et al, 2012; Zhang et al, 2013; Koh et al, 2014)

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