Putative Neural Network Within an Olfactory Sensory Unit for Nestmate and Non-nestmate Discrimination in the Japanese Carpenter Ant: The Ultra-structures and Mathematical Simulation.

Yusuke Takeichi,Yasuhisa Endo,Jo Takano,Mamiko Ozaki,Kazuyoshi Murata,Eichi Takaya,Naoko Kajimura,Toshiaki Omori,Tatsuya Uebi,Satoshi Kurihara,Koichi Ozaki,Kouji Yasuyama,Naoyuki Miyazaki,Toshinobu Suzaki,Masaru K Hojo,Ryoichi Yoshimura,Hideo Kubo,Kanako Inoue,Kenta Tatsuta

doi:10.3389/fncel.2018.00310

Abstract

Ants are known to use a colony-specific blend of cuticular hydrocarbons (CHCs) as a pheromone to discriminate between nestmates and non-nestmates and the CHCs were sensed in the basiconic type of antennal sensilla (S. basiconica). To investigate the functional design of this type of antennal sensilla, we observed the ultra-structures at 2D and 3D in the Japanese carpenter ant, Camponotus japonicus, using a serial block-face scanning electron microscope (SBF-SEM), and conventional and high-voltage transmission electron microscopes. Based on the serial images of 352 cross sections of SBF-SEM, we reconstructed a 3D model of the sensillum revealing that each S. basiconica houses > 100 unbranched dendritic processes, which extend from the same number of olfactory receptor neurons (ORNs). The dendritic processes had characteristic beaded-structures and formed a twisted bundle within the sensillum. At the “beads,” the cell membranes of the processes were closely adjacent in the interdigitated profiles, suggesting functional interactions via gap junctions (GJs). Immunohistochemistry with anti-innexin (invertebrate GJ protein) antisera revealed positive labeling in the antennae of C. japonicus. Innexin 3, one of the five antennal innexin subtypes, was detected as a dotted signal within the S. basiconica as a sensory organ for nestmate recognition. These morphological results suggest that ORNs form an electrical network via GJs between dendritic processes. We were unable to functionally certify the electric connections in an olfactory sensory unit comprising such multiple ORNs; however, with the aid of simulation of a mathematical model, we examined the putative function of this novel chemosensory information network, which possibly contributes to the distinct discrimination of colony-specific blends of CHCs or other odor detection.

Highlights

The natural environment surrounding living organisms is filled with chemical information, and animals have developed adaptive chemosensory systems to utilize this environmental information for purposes such as food source or mate recognition or individual identification especially in social animals
The receptor membranes of olfactory receptor neurons (ORNs) are surrounded by chemosensory protein (CSP)-containing sensillar lymph, allowing lipophilic cuticular hydrocarbons (CHCs) to be transported by CSP to the receptor membranes of ORNs (Ozaki et al, 2005; Hojo et al, 2015)
Its complexity is dependent on the repertoire of related olfactory receptor (OR) genes belonging to the 9-exon subfamily (Engsontia et al, 2015; Zhou et al, 2015; McKenzie et al, 2016; Pask et al, 2017; Slone et al, 2017), which are expressed in the S. basiconica ORNs projecting the same number of glomeruli in a specific antennal lobe region called T6 (Zube et al, 2008; Kelber et al, 2010; Nakanishi et al, 2010; Nishikawa et al, 2012; Kropf et al, 2014; McKenzie et al, 2016; Couto et al, 2017)

Summary

Introduction

The natural environment surrounding living organisms is filled with chemical information, and animals have developed adaptive chemosensory systems to utilize this environmental information for purposes such as food source or mate recognition or individual identification especially in social animals. Many insect species use sex pheromones for attracting mates, and their sex pheromonesensitive sensilla, which house a few olfactory receptor neurons (ORNs), have been enthusiastically studied as simple odor sensory units (Kaissling, 1987; Haupt et al, 2010). Worker ants utilize a colony-specific blend of cuticular hydrocarbons (CHCs) as a social pheromone for nestmate recognition (Vander Meer, 1998; Lahav et al, 1999; Ozaki et al, 2005; Brandstaetter et al, 2008; Guerrieri and d’Ettorre, 2008; Guerrieri et al, 2009; Nick and d’Ettorre, 2012; Ozaki and Hefetz, 2014). It is considered that the S. basiconica of ant probably classified into subtypes would be multifunctional olfactory organ for nestmate and non-nestmate discrimination and for other hydrocarbon or general odor sensing as in other insects (Kropf et al, 2014; Couto et al, 2017)

Methods

Results

Conclusion