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Interspecific introgressive origin of genomic diversity in the house mouse

Significance The mouse has been one of the main mammalian model organisms used for genetic and biomedical research. Understanding the evolution of house mouse genomes would shed light not only on genetic interactions and their interplay with traits in the mouse but would also have significant implications for human genetics and health. Analysis using a recently developed statistical method shows that the house mouse genome is a mosaic that contains previously unrecognized contributions from a different mouse species. We traced these contributions to ancient and recent interbreeding events. Our findings reveal the extent of introgression in an important mammalian genome and provide an approach for genome-wide scans of introgression in other eukaryotic genomes. We report on a genome-wide scan for introgression between the house mouse (Mus musculus domesticus) and the Algerian mouse (Mus spretus), using samples from the ranges of sympatry and allopatry in Africa and Europe. Our analysis reveals wide variability in introgression signatures along the genomes, as well as across the samples. We find that fewer than half of the autosomes in each genome harbor all detectable introgression, whereas the X chromosome has none. Further, European mice carry more M. spretus alleles than the sympatric African ones. Using the length distribution and sharing patterns of introgressed genomic tracts across the samples, we infer, first, that at least three distinct hybridization events involving M. spretus have occurred, one of which is ancient, and the other two are recent (one presumably due to warfarin rodenticide selection). Second, several of the inferred introgressed tracts contain genes that are likely to confer adaptive advantage. Third, introgressed tracts might contain driver genes that determine the evolutionary fate of those tracts. Further, functional analysis revealed introgressed genes that are essential to fitness, including the Vkorc1 gene, which is implicated in rodenticide resistance, and olfactory receptor genes. Our findings highlight the extent and role of introgression in nature and call for careful analysis and interpretation of house mouse data in evolutionary and genetic studies.