Abstract
Assortative mating, a potentially efficient prezygotic reproductive barrier, may prevent loss of genetic potential by avoiding the production of unfit hybrids (i.e., because of hybrid infertility or hybrid breakdown) that occur at regions of secondary contact between incipient species. In the case of the mouse hybrid zone, where two subspecies of Mus musculus (M. m. domesticus and M. m. musculus) meet and exchange genes to a limited extent, assortative mating requires a means of subspecies recognition. We based the work reported here on the hypothesis that, if there is a pheromone sufficiently diverged between M. m. domesticus and M. m. musculus to mediate subspecies recognition, then that process must also require a specific receptor(s), also sufficiently diverged between the subspecies, to receive the signal and elicit an assortative mating response. We studied the mouse V1R genes, which encode a large family of receptors in the vomeronasal organ (VNO), by screening Perlegen SNP data and identified one, Vmn1r67, with 24 fixed SNP differences most of which (15/24) are nonsynonymous nucleotide substitutions between M. m. domesticus and M. m. musculus. We observed substantial linkage disequilibrium (LD) between Vmn1r67 and Abpa27, a mouse salivary androgen-binding protein gene that encodes a proteinaceous pheromone (ABP) capable of mediating assortative mating, perhaps in conjunction with its bound small lipophilic ligand. The LD we observed is likely a case of association rather than residual physical linkage from a very recent selective sweep, because an intervening gene, Vmn1r71, shows significant intra(sub)specific polymorphism but no inter(sub)specific divergence in its nucleotide sequence. We discuss alternative explanations of these observations, for example that Abpa27 and Vmn1r67 are coevolving as signal and receptor to reinforce subspecies hybridization barriers or that the unusually divergent Vmn1r67 allele was not a product of fast positive selection, but was derived from an introgressed allele, possibly from Mus spretus.
Highlights
Pheromones, specific substances secreted to the exterior of an organism, communicate information about sex, species and related states to other members of the same species, whereupon the pheromones elicit specific reactions such as behavior and/or endocrine changes [1]
We began our search for a V1R gene(s) with different haplotypes fixed in the two subspecies, M. m. domesticus and M. m. musculus, by screening the 392 V1R genes for those with the most SNP differences between the wild-derived inbred strains WSB and PWD in the Perlegen SNP data [50]
To determine how many SNPs in these candidate V1R genes might represent fixed nucleotide differences between the two subspecies of interest, we produced DNA sequences of the ten top-ranked genes from the Perlegen screen in at least two wild-derived inbred strains of each subspecies
Summary
Pheromones, specific substances secreted to the exterior of an organism, communicate information about sex, species and related states to other members of the same species, whereupon the pheromones elicit specific reactions such as behavior and/or endocrine changes [1]. Olfactory cues represent the primary means of communication in nocturnal animals such as the house mouse [4,5] and two families of receptors in the vomeronasal organ (VNO), the V1Rs and the V2Rs, are thought to detect pheromonal signals [6]. In the case of putative mouse pheromones, receptor identification has generally relied on cell biology experiments which have indicated that the VNO and the accessory olfactory bulb comprise the system receiving and processing the information [7,8], but in those experiments identification of the specific VNO receptors has been elusive. We demonstrate a purely genetic and evolutionary approach with which to identify specific receptors for a particular pheromonal function, subspecies recognition [9,10,11], thought to mediate assortative mating where two different subspecies make secondary contact, e.g. the European house mouse hybrid zone described below
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