Divergent V1R repertoires in five species: Amplification in rodents, decimation in primates, and a surprisingly small repertoire in dogs

Abstract

The V1R gene family comprises one of two types of putative pheromone receptors expressed in the mammalian vomeronasal organ (VNO). We searched the most recent mouse, rat, dog, chimpanzee, and human genome sequence assemblies to compile a near-complete repertoire of V1R genes for each species. Dog, human, and chimpanzee have very few intact V1Rs (8, 2, and 0, respectively) compared to more than a hundred intact V1Rs in each of the rat (106) and mouse (165) genomes. We also provide the first description of the diversity of V1R pseudogenes in these species. We identify at least 165 pseudogenes in mouse, 110 in rat, 102 in chimpanzee, 115 in human, and 54 in dog. Primate and dog pseudogenes are distributed among almost all V1R subfamilies seen in rodents, indicating that the common ancestor of these species had a diverse V1R repertoire. We find that V1R genes were subject to strikingly different fates in different species and in different subfamilies. In rodents, some subfamilies remained relatively stable or underwent roughly equivalent expansion in mouse and rat; other subfamilies expanded in one species but not the other. The small number of intact V1Rs in the dog genome is unexpected given the presumption that dogs, like rodents, have a functional VNO, and a complex system of pheromone-based behaviors. We identify an intact transient receptor potential channel 2beta in the dog genome, consistent with a functional VNO in dogs. The diminished V1R repertoire in dogs raises questions about the relative contributions of V1Rs versus other candidate pheromone receptor genes in the establishment of complex pheromone systems in mammals.

Figure 1.

Neighbor-joining gene tree based on nucleotide alignments illustrating subfamily representation (A-L) of intact mouse (red), rat (blue), dog (green), and human (brown) V1Rs. Three dog V1Rs and one mouse V1R that could be pseudogenes (see Methods) are indicated with asterisks.

Figure 2.

Neighbor-joining gene tree illustrating subfamily clades (A-L, P) of intact and pseudogene V1R-like sequences identified in the genomes of five mammalian species. Mouse intact (red), mouse pseudogene (red dashed), rat intact (blue), rat pseudogene (blue dashed), dog intact (green), dog pseudogene (green dashed), human intact (brown, denoted “h”), and human/chimpanzee pseudogene (yellow dashed) branches are shown. Two chimpanzee and three human pseudogenes that were previously annotated as intact V1Rs (see Methods) are indicated with yellow and orange asterisks, respectively. A total of 87 mouse, 39 rat, 27 dog, 59 chimpanzee, and 58 human V1R-like pseudogenes were excluded from this tree, because the length of confidently aligned sequence was too short (see Methods). A list of these excluded sequences, as well as their presumed subfamily (based on closest fast×34 matches), is provided in Supplemental Figure D.