Olfactory pathway of the hornet Vespa velutina: New insights into the evolution of the hymenopteran antennal lobe

Abstract

In the course of evolution, eusociality has appeared several times independently in Hymenoptera, within different families such as Apidae (bees), Formicidae (ants), and Vespidae (wasps and hornets), among others. The complex social organization of eusocial Hymenoptera relies on sophisticated olfactory communication systems. Whereas the olfactory systems of several bee and ant species have been well characterized, very little information is as yet available in Vespidae, although this family represents a highly successful insect group, displaying a wide range of life styles from solitary to eusocial. Using fluorescent labeling, confocal microscopy, and 3D reconstructions, we investigated the organization of the olfactory pathway in queens, workers, and males of the eusocial hornet Vespa velutina. First, we found that caste and sex dimorphism is weakly pronounced in hornets, with regard to both whole-brain morphology and antennal lobe organization, although several male-specific macroglomeruli are present. The V. velutina antennal lobe contains approximately 265 glomeruli (in females), grouped in nine conspicuous clusters formed by afferent tract subdivisions. As in bees and ants, hornets display a dual olfactory pathway, with two major efferent tracts, the medial and the lateral antennal lobe tracts (m- and l-ALT), separately arborizing two antennal lobe hemilobes and projecting to partially different regions of higher order olfactory centers. Finally, we found remarkable anatomical similarities in the glomerular cluster organizations among hornets, ants, and bees, suggesting the possible existence of homologies in the olfactory pathways of these eusocial Hymenoptera. We propose a common framework for describing AL compartmentalization across Hymenoptera and discuss possible evolutionary scenarios. J. Comp. Neurol. 524:2335-2359, 2016. © 2016 Wiley Periodicals, Inc.

Hornets Have It: A Conserved Olfactory Subsystem for Social Recognition in Hymenoptera?

“…These olfactory sensory tracts, termed T A – T I (Couto et al, 2016), innervate nine distinct clusters of glomeruli, with similar innervation pattern in males and females (Figure 3). We investigated the projection pattern of sensory neurons from basiconic sensilla 2, using specific single sensillum staining.…”

“…The antennal lobes are represented as seen from the ventral side (C,D) or the dorsal side (E,F) . The V. velutina antennal lobe contains nine glomerular clusters termed T A – T I (color coded in C–F ) in both females and males (Couto et al, 2016). The T B cluster is formed by a tight group of small glomeruli in the dorso-caudal region of the antennal lobe.…”

“…Neuroanatomical studies have pointed out striking similarities in AL organization across different Hymenoptera, especially concerning the division of the antennal nerve in different tracts projecting into distinct clusters of glomeruli (Zube et al, 2008; Nishino et al, 2009; Couto et al, 2016). A currently debated question is whether morphologically similar AL clusters across different species are indicative of conserved olfactory structures (homologous clusters), or if they are the result of convergent evolution.…”

“…Indeed, in both species sensory neurons of basiconic sensilla exclusively project into a dorso-caudal cluster containing numerous small glomeruli (Nakanishi et al, 2009, 2010; Kelber et al, 2010). Olfactory information processed within this subsystem is further conveyed to higher-order centers by the median tract of uniglomerular projection neurons (m-ALT) in ants as well as in wasps (Zube et al, 2008; Couto et al, 2016). In addition to similar input-output connectivity, the rare immunoreactive profile of this glomerular cluster suggests that innervations of local AL neurons are alike.…”

Hydrocarbons mediate seed dispersal: a new mechanism of vespicochory

“…Additionally, insect chemosensory proteins (CSPs) have been proposed as carriers to transport chemical stimuli through the sensillar lymph and deliver them to the olfactory receptors (Hansson & Stensmyr, ). Recent studies also report that sensory neurons within the basiconic sensilla of V. velutina preferentially respond to hydrocarbons (Couto et al ., , ). This current study showed that two CSP genes were mainly expressed in the antennae, whereas there was low expression in other tissues (Fig.…”