Abstract
The vomeronasal organ (VNO) is functional in most terrestrial mammals, though progressively reduced in the primate lineage, and is used for intraspecific communication and predator recognition. Vomeronasal receptor (VR) genes comprise two families of chemosensory genes (V1R and V2R) that have been considered to be specific for the VNO. However, recently a large number of VRs were reported to be expressed in the main olfactory epithelium (MOE) of mice, but there is little knowledge of the expression of these genes outside of rodents. To explore the function of VR genes in mammalian evolution, we analyzed and compared the expression of 64 V1R and 2 V2R genes in the VNO and the MOE of the gray mouse lemur (Microcebus murinus), the primate with the largest known VR repertoire. We furthermore compared expression patterns in adults of both sexes and seasons, and in an infant. A large proportion (83–97%) of the VR loci was expressed in the VNO of all individuals. The repertoire in the infant was as rich as in adults, indicating reliance on olfactory communication from early postnatal development onwards. In concordance with mice, we also detected extensive expression of VRs in the MOE, with proportions of expressed loci in individuals ranging from 29 to 45%. TRPC2, which encodes a channel protein crucial for signal transduction via VRs, was co-expressed in the MOE in all individuals indicating likely functionality of expressed VR genes in the MOE. In summary, the large VR repertoire in mouse lemurs seems to be highly functional. Given the differences in the neural pathways of MOE and VNO signals, which project to higher cortical brain centers or the limbic system, respectively, this raises the intriguing possibility that the evolution of MOE-expression of VRs enabled mouse lemurs to adaptively diversify the processing of VR-encoded olfactory information.
Highlights
Most terrestrial mammals use two olfactory systems, the main olfactory system based on the main olfactory epithelium (MOE) and the accessory olfactory system based on the vomeronasal organ (VNO)
Two types of vomeronasal receptors (VRs) are described which have been thought to be primarily expressed in the VNO based on studies in rodents: vomeronasal 1 receptors (V1Rs, Dulac and Axel, 1995) and vomeronasal 2 receptors
If maxilloturbinal tissue was not contaminated with VNO cells during its removal, we assume that MOE tissue was not contaminated with VNO cells and potential expression patterns of VRs in MOE tissue shown in this study relate to actual expression in the MOE
Summary
Most terrestrial mammals use two olfactory systems, the main olfactory system based on the main olfactory epithelium (MOE) and the accessory olfactory system based on the vomeronasal organ (VNO). A recent study using nano Cap Analysis of Gene Expression revealed the expression of a large proportion of VRs in the mouse MOE (112 of 191 tested V1Rs and 96 of 123 V2Rs; Pascarella et al, 2014). Both types of VRs use the cation channel TRPC2 (Transient Receptor Potential channel type C2) in the signal transduction pathway (Liman et al, 1999). One study did not find TRPC2 expression outside of the mouse VNO (Zhang et al, 2010), another study reported a very faint signal for TRPC2 in the MOE on Northern blots and a faint signal in a small population of MOE
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