Irregular vomeronasal system of hedgehogs is intermediate between segregated and uniform: how was type-2 receptor (V2R)-pathway in Laurasiatheria lost during evolution?

Abstract

Most mammals detect important specific chemicals such as pheromones via the vomeronasal system (VNS). The types-1 (V1R) and -2 (V2R) families of vomeronasal receptors detect volatile and water-soluble substances, respectively, and couple with G protein α subunits i2 (Gαi2) and o (Gαo), respectively. The V1R/Gαi2- and V2R/Gαo-neurons in the vomeronasal organ (VNO), respectively project to the anterior and posterior halves of the accessory olfactory bulb (AOB) (i.e. segregated type) in rodents and some other mammalian species. In contrast, the VNO in most species in the Laurasiatheria clade contains only V1R/Gαi2-neurons that project to the entire AOB (i.e. uniform type). Considering the above, the posterior pathway for identifying specific emitters via the V2R families might have disappeared from the Laurasiatheria clade. Here, we analyzed the VNS of hedgehogs, one of the earliest divergent groups in the Laurasiatheria clade. In the African pigmy hedgehog (Atelerix albiventris), immunohistochemical staining using antibodies against Gαi2 and Gαo revealed that the VNO contains V1R/Gαi2- and V2R/Gαo-neurons. The vomeronasal nerve and glomerular layers of the hedgehog AOB were positive for Gαi2, and the posterior half was also positive for Gαo. This profile is intermediate between the segregated and uniform types of the mammalian VNS. Dual immunofluorescence staining also indicated that the posterior glomeruli of the hedgehog AOB comprised mixtures of V1R/Gαi2- and V2R/Gαo-axons. These features of the hedgehog VNS seem to reflect the process of evolutionary disappearance of V2R-pathway within Laurasiatheria.