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. 2014 Sep;357(3):583-95.
doi: 10.1007/s00441-014-1892-y. Epub 2014 May 13.

Olfactory subsystems in the honeybee: sensory supply and sex specificity

Affiliations

Olfactory subsystems in the honeybee: sensory supply and sex specificity

Jan Kropf et al. Cell Tissue Res. 2014 Sep.

Abstract

The antennae of honeybee (Apis mellifera) workers and drones differ in various aspects. One striking difference is the presence of Sensilla basiconica in (female) workers and their absence in (male) drones. We investigate the axonal projection patterns of olfactory receptor neurons (ORNs) housed in S. basiconica in honeybee workers by using selective anterograde labeling with fluorescent tracers and confocal-microscopy analysis of axonal projections in antennal lobe glomeruli. Axons of S. basiconica-associated ORNs preferentially projected into a specific glomerular cluster in the antennal lobe, namely the sensory input-tract three (T3) cluster. T3-associated glomeruli had previously been shown to be innervated by uniglomerular projection (output) neurons of the medial antennal lobe tract (mALT). As the number of T3 glomeruli is reduced in drones, we wished to determine whether this was associated with the reduction of glomeruli innervated by medial-tract projection neurons. We retrogradely traced mALT projection neurons in drones and counted the innervated glomeruli. The number of mALT-associated glomeruli was strongly reduced in drones compared with workers. The preferential projections of S. basiconica-associated ORNs in T3 glomeruli together with the reduction of mALT-associated glomeruli support the presence of a female (worker)-specific olfactory subsystem that is partly innervated by ORNs from S. basiconica and is associated with the T3 cluster of glomeruli and mALT projection neurons. We propose that this olfactory subsystem supports parallel olfactory processing related to worker-specific olfactory tasks such as the coding of colony odors, colony pheromones and/or odorants associated with foraging on floral resources.

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Figures

Fig. 1
Fig. 1
Light microscopic images of Sensilla basiconica (Sb), Sensilla placodea (Sp) and Sensilla trichoidea (St., St) on a honeybee worker antenna. a Overview of the ninth segment. Bar 100 μm. b Detailed view of the S. basiconica-rich region on the ninth segment (white asterisks bases of two identifiable S. basiconica). Bar 25 μm
Fig. 2
Fig. 2
a Z-projection of a double-mass-staining of hair-like sensilla on segment 9 (magenta) and segment 4 (green) of honey bee antenna. The input tracts T1 and T3 are indicated. Note the two sorting zones (SZ1, SZ2). Bar 100 μm. Insets Detailed views of two glomeruli that are innervated by axons from olfactory receptor neurons from both the distal and the proximal parts of segment 9 in a layered fashion. Bar 25 μm. b Z-projection of an antennal lobe with an intracellularly stained projection neuron innervating a single glomerulus. Bar 100 μm. Inset Stained glomerulus in more detail; the dendritic arborizations of a projection neuron ramify throughout the entire glomerulus. Bar 25 μm
Fig. 3
Fig. 3
Images of a representative mass-staining of the axons of olfactory receptor neurons in Sensilla trichoidea of segment 5 of the honeybee worker antenna. Axons of olfactory receptor neurons are shown in magenta; the background was visualized via autofluorescence of the tissue and is shown in green. a Z-projection of 20 μm of the dorsal part of the stained antennal lobe; the glomeruli innervated from T1 input tract (T1) are clearly visible. b Z-projection of 20 μm of the dorsal middle part of the stained antennal lobe. Glomeruli innervated from the T3 input tract (T3) and the T1 input tract (T1) are clearly visible. c Z-projection of 20 μm of the ventral middle part of the stained antennal lobe. Glomeruli innervated from the T3 input tract (T3) and the T2 input tract (T2) are clearly visible. d Z-projection of 20 μm of the ventral part of the stained antennal lobe. Glomeruli innervated from the T3 input tract (T3) are clearly visible; the only non-innervated glomeruli (probably associated with T4 input tract) are indicated by the dashed circle. Bar 200 μm
Fig. 4
Fig. 4
Confocal image stacks from two antennal lobes after staining of Sensilla basiconica-rich regions of the antenna (a–f) and image stacks of a single-sensillum staining of a S. basiconicum (g–i). Stained glomeruli (asterisks). a, d, g Complete stacks of antennal lobes with the antennal nerves (AN) and olfactory receptor neuron (ORN) arborizations in single glomeruli can hardly be identified in the complete image stacks. Bar 100 μm. b, e, h Substacks of the antennal lobes with identifiable ORN innervation in individual glomeruli in the T1 glomerular cluster. c, f, i Substacks of the antennal lobe with identifiable ORN innervation in individual glomeruli in the T3 glomerular cluster region. Bar 100 μm
Fig. 5
Fig. 5
Numbers of glomeruli containing axonal projections from selective staining of ORNs in multiple Sensilla basiconica. Antennal lobe input tract T3 glomeruli were stained significantly more often compared with T1 glomeruli and T1 glomeruli were stained more often than T2 and T4 glomeruli (Friedman ANOVA, post-hoc Wilcoxon rank sum test with Bonferroni correction for multiple comparisons, n = 15, A–C significant differences between clusters)
Fig. 6
Fig. 6
a Z-projection of a mass-staining of antennal lobe (AL) projection neurons in the honeybee drone; the AL, the medial and the lateral AL tract (mALT, lALT) and arborizations in the mushroom bodies (MB) and the lateral horn (LH) are visible. Bar 200 μm. b Z-projection of mALT staining in a honeybee drone. The axons, cell bodies (CB) and dendritic glomerular (GL) innervation are visible. Bar 100 μm. c Three-dimensional reconstruction of a drone AL with the antennal nerve (AN) after staining of all olfactory receptor neuron axons. Two macroglomeruli (MGL) are indicated. d Reconstruction of the mALT proportion of glomeruli and two macroglomeruli (MGL) within the T1 glomerular cluster (T1) as landmarks in a drone AL. The two lALT-associated MGL are shown in green, whereas mALT glomeruli in the T3 glomerular cluster (T3) are shown in shades of magenta. Bar 100 μm
Fig. 7
Fig. 7
Representations of a honeybee worker (left) and drone (right) antennal lobe (AL). Olfactory receptor neuron axons housed in S. basiconica are only present in workers and project via the antennal nerve mainly to the T3 glomerular cluster (T3) in the AL (light blue projections). The T1 glomerular cluster (T1) is drawn in shades of green, the T2 in shades of yellow (T2) and the T4 cluster in shades of blue (T4). The medial AL tract (mALT) innervates mainly T3 glomeruli and the lateral AL tract (lALT) mainly T1 glomeruli. The T3 glomerular cluster and the mALT output tract are reduced in drones. The estimated numbers of glomeruli innervated by mALT and lALT projection neurons and the total numbers of glomeruli in the female (from Kirschner et al. 2006) and male AL are indicated (ORNs olfactory receptor neurons)

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