Abstract
In most animal species, the vomeronasal organ ensures the individual recognition of conspecifics, a prerequisite for a successful reproduction. The vomeronasal organ expresses several receptors for pheromone detection. Mouse vomeronasal type-2 receptors (V2Rs) are restricted to the basal neurons of this organ and organized in four families. Family-A, B and D (family ABD) V2Rs are expressed monogenically (one receptor per neuron) and coexpress with either Vmn2r1 or Vmn2r2, two members of family-C V2Rs. Thus, basal neurons are characterized by specific combinations of two V2Rs. To investigate this issue, we raised antibodies against all family-C V2Rs and analyzed their expression pattern. We found that six out of seven family-C V2Rs (Vmn2r2-7) largely coexpressed and that none of the anti-Vmn2r2-7 antibodies significantly stained Vmn2r1 positive neurons. Thus, basal neurons are divided into two complementary subsets. The first subset (Vmn2r1-positive) preferentially coexpresses a distinct group of family-ABD V2Rs, whereas the second subset (Vmn2r2-7-positive) coexpresses the remaining group of V2Rs. Phylogenetic reconstruction and the analysis of genetic loci in various species reveal that receptors expressed by this second neuronal subset are recent branches of the V2R tree exclusively present in mouse and rat. Conversely, V2Rs expressed in Vmn2r1 positive neurons, are phylogenetically ancient and found in most vertebrates including rodents. Noticeably, the more recent neuronal subset expresses a type of Major Histocompatibility Complex genes only found in murine species. These results indicate that the expansion of the V2R repertoire in a murine ancestor occurred with the establishment of a new population of vomeronasal neurons in which coexists the polygenic expression of a recent group of family-C V2Rs (Vmn2r2-7) and the monogenic expression of a recent group of family-ABD V2Rs. This evolutionary innovation could provide a molecular rationale for the exquisite ability in individual recognition and mate choice of murine species.
Highlights
Success in reproduction is strongly dependent on individual recognition
Expression pattern of family-C vomeronasal type-2 receptors (V2Rs) In a previous paper, we reported that Vmn2r1 and Vmn2r2 expression defines two distinct populations of neurons in the basal layer of the mouse vomeronasal organ (VNO) that in total represent about 85% of all basal cells
This observation led to the conclusions that Vmn2r1 and Vmn2r2 are mutually exclusively expressed in the VNO neurons, suggesting that such a modality of expression could be extended to all family-C receptors, namely Vmn2r1-7 (Figure 1)
Summary
Success in reproduction is strongly dependent on individual recognition. In most species, pheromone detecting systems ensures that animals recognize individual conspecifics but can scrutinize their social and reproductive status [1].Rodents, in particular, possess a well developed accessory olfactory organ, the vomeronasal organ (VNO), that triggers pheromone-mediated behavioral and neuroendocrine responses, both essential features for a successful mating rate [1]. Intraspecies recognition and successful reproduction in harsh environments are key factors for the worldwide spreading of some rodent species such as mouse and rat. Hundreds of receptors, included in three distinct G-protein coupled receptor superfamilies, have been reportedly expressed in chemosensory neurons of this accessory olfactory organ [4,5,6,7,8,9]. Each of these receptor superfamilies is expressed in only one of two large neuronal subsets, referred to as apical and basal that project to two distinct and non-overlapping regions of the AOB, suggesting a dichotomic modality to elaborate the pheromonal signal [10,11]
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