Arboreal Squirrels Have a Segregated Vomeronasal System With a Regressed Type 2 Receptor (V2R)-Domain

The vomeronasal system (VNS) in most mammals detects species-specific chemicals. Vomeronasal type 1 (V1R) and type 2 (V2R) receptors in the VNS, respectively, couple with G protein α subunits i2 (Gαi2) and o (Gαo). Most artiodactyls and carnivores have neurons that express only V1R/Gαi2 in the peripheral vomeronasal organ and project axons to the entire accessory olfactory bulb (AOB) (uniform type). In contrast, most rodents have V1R/Gαi2 and V2R/Gαo-neurons that respectively project to the rostral and caudal parts of the AOB (segregated type). However, the California ground squirrel (Otospermophilus beecheyi; family Sciuridae, subfamily Xerinae) has a V1R/Gαi2 AOB, which is the only exception to the segregated profiles of rodents to date. Here, we immunohistochemically analyzed the AOBs of four Pallas's (Callosciurus erythraeus; subfamily Callosciurinae) and three Eurasian red (Sciurus vulgaris; subfamily Sciurinae) squirrels using anti-Gαi2 and anti-Gαo antibodies. The AOBs of both arboreal species consisted of the vomeronasal nerve (VNL), glomerular (GL), external cellular (ECL), and internal cellular (ICL) layers. We found both Gαi2- and Gαo-positive regions in the VNL and GL in all squirrels examined in this study, which suggested that they can detect nonvolatile cues as pheromones or kairomones via V2R like rodents in general. However, the V1R/Gαi2 and V2R/Gαo domains were not equivalent in the AOBs of these squirrels, as a large area corresponded to the V1R/Gαi2-domain. Considering these results together with findings from ground squirrels, V2R expression in the VNS seems to be reduced in the family Sciuridae among rodents.