Interspecific variation of antennal lobe composition among four hornet species

Antoine Couto,Hiroyuki Ai,Gérard Arnold,Jean-Christophe Sandoz

doi:10.1038/s41598-021-00280-z

Abstract

Olfaction is a crucial sensory modality underlying foraging, social and mating behaviors in many insects. Since the olfactory system is at the interface between the animal and its environment, it receives strong evolutionary pressures that promote neuronal adaptations and phenotypic variations across species. Hornets are large eusocial predatory wasps with a highly developed olfactory system, critical for foraging and intra-specific communication. In their natural range, hornet species display contrasting ecologies and olfactory-based behaviors, which might match to adaptive shifts in their olfactory system. The first olfactory processing center of the insect brain, the antennal lobe, is made of morphological and functional units called glomeruli. Using fluorescent staining, confocal microscopy and 3D reconstructions, we compared antennal lobe structure, glomerular numbers and volumes in four hornet species (Vespa crabro, Vespa velutina, Vespa mandarinia and Vespa orientalis) with marked differences in nesting site preferences and predatory behaviors. Despite a conserved organization of their antennal lobe compartments, glomeruli numbers varied strongly between species, including in a subsystem thought to process intraspecific cuticular signals. Moreover, specific adaptations involving enlarged glomeruli appeared in two species, V. crabro and V. mandarinia, but not in the others. We discuss the possible function of these adaptations based on species-specific behavioral differences.

Highlights

All these examples show that phylogenetically close species, such as different Vespa species, can acquire different behavioural traits to deal with specific ecological challenges
Odorant molecules are detected by olfactory sensory neurons (OSN) on the antennae, which project to a primary olfactory structure, the antennal lobe[27] (AL)
The AL of social Hymenoptera stands out as complex as it contains a high number of glomeruli, compartmentalized in clusters formed by distinct bundles of OSN a xons[52,53,54,55,56]

Summary

Introduction

All these examples show that phylogenetically close species, such as different Vespa species, can acquire different behavioural traits to deal with specific ecological challenges. Odorant molecules are detected by olfactory sensory neurons (OSN) on the antennae, which project to a primary olfactory structure, the antennal lobe[27] (AL). This structure is made of morphological and functional units called glomeruli, which individually gather inputs from a given type of OSN28–30. We addressed this question in the Vespidae, by comparing the antennal lobe organization of four hornet species of the genus Vespa These species differ in ecology, nesting site preference and predatory behavior, which may have given rise to diverse neuronal adaptations in their olfactory system. We measured and compared across species the volumes of glomeruli, asking if macroglomeruli exist in the AL of workers

Objectives

Results

Conclusion