Abstract
BackgroundThe mammalian vomeronasal organ (VNO) expresses two G-protein coupled receptor gene families that mediate pheromone responses, the V1R and V2R receptor genes. In rodents, there are ~150 V1R genes comprising 12 subfamilies organized in gene clusters at multiple chromosomal locations. Previously, we showed that several of these subfamilies had been extensively modulated by gene duplications, deletions, and gene conversions around the time of the evolutionary split of the mouse and rat lineages, consistent with the hypothesis that V1R repertoires might be involved in reinforcing speciation events. Here, we generated genome sequence for one large cluster containing two V1R subfamilies in Mus spretus, a closely related and sympatric species to Mus musculus, and investigated evolutionary change in these repertoires along the two mouse lineages.ResultsWe describe a comparison of spretus and musculus with respect to genome organization and synteny, as well as V1R gene content and phylogeny, with reference to previous observations made between mouse and rat. Unlike the mouse-rat comparisons, synteny seems to be largely conserved between the two mouse species. Disruption of local synteny is generally associated with differences in repeat content, although these differences appear to arise more from deletion than new integrations. Even though unambiguous V1R orthology is evident, we observe dynamic modulation of the functional repertoires, with two of seven V1Rb and one of eleven V1Ra genes lost in spretus, two V1Ra genes becoming pseudogenes in musculus, two additional orthologous pairs apparently subject to strong adaptive selection, and another divergent orthologous pair that apparently was subjected to gene conversion.ConclusionTherefore, eight of the 18 (~44%) presumptive V1Ra/V1Rb genes in the musculus-spretus ancestor appear to have undergone functional modulation since these two species diverged. As compared to the rat-mouse split, where modulation is evident by independent expansions of these two V1R subfamilies, divergence between musculus and spretus has arisen more by mutations within coding sequences. These results support the hypothesis that adaptive changes in functional V1R repertoires contribute to the delineation of very closely related species.
Highlights
The mammalian vomeronasal organ (VNO) expresses two G-protein coupled receptor gene families that mediate pheromone responses, the V1R and V2R receptor genes
The G protein-coupled receptors (GPCRs) repertoire has a common seven transmembrane structure, and mammalian GPCR proteins are classified into six major families: the peptide-binding secretin types, the adhesion types that contain N-terminal domains with motifs implicated in cell adhesion functions (e.g., EGF-like repeats), the glutamate types, the frizzled types, the Taste2 types (TAS2 taste receptors), and the large set of rhodopsin types [6]
The genome features of this locus resemble the syntenic locus in Mus musculus, including a comparable number of V1R genes with little evidence for gene duplication/deletion, organized in a comparably sized region flanked by the same non-V1R genes on either side
Summary
The mammalian vomeronasal organ (VNO) expresses two G-protein coupled receptor gene families that mediate pheromone responses, the V1R and V2R receptor genes. The vomeronasal organ (VNO) of terrestrial vertebrates is responsible for pheromonal responses that evoke social and reproductive behaviors, including male territorial aggression, sexual preference, and sexual maturity (reviewed in [1]). These responses are thought to be mediated by at least two unrelated gene families, referred to as V1Rs [2] and V2Rs [3,4,5], encoding G protein-coupled receptors (GPCRs) that are expressed on surfaces of sensory neurons in the VNO. V1Rs share a distant relationship with the Taste2- and rhodopsin-types of GPCRs that bind ligands within transmembrane cavities (and that lack the large N-terminal binding domains characteristic of other GPCRs)
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