Interspecific introgressive origin of genomic diversity in the house mouse

Abstract

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.Mus musculus | Mus spretus | hybridization | adaptive introgression | PhyloNet-HMM C lassical laboratory mouse strains, as well as newly established wild-derived ones, are widely used by geneticists for answering a diverse array of questions (1). Understanding the genome contents and architecture of these strains is important for studies of natural variation and complex traits, as well as evolutionary studies in general (2). Mus spretus, a sister species of Mus musculus, impacts the findings in M. musculus investigations for at least two reasons. First, it was deliberately interbred with laboratory M. musculus strains to introduce genetic variation (3). Second, Mus musculus domesticus is partially sympatric (naturally cooccurring) with M. spretus (Fig. 1).Recent studies have examined admixture between subspecies of house mice (5-8), but have not studied introgression with M. spretus. In at least one case (5), the introgressive descent of the mouse genome was hidden due to data postprocessing that masked introgressed genomic regions as missing data. In another study reporting whole-genome sequencing of 17 classical laboratory strains (6), M. spretus was used as an outgroup for phylogenetic analysis. The authors were surprised to find that 12.1% of loci failed to place M. spretus as an outgroup to the M. musculus clade. The authors concluded that M. spretus was not a reliable outgroup but did not pursue their observation further. On the other hand, in a 2002 study (9), Orth et al. compiled data on allozyme, microsatellite, and mitochondrial variation in house mice from Spain (sympatry) and...

Phylogenomic Insights into Mouse Evolution Using a Pseudoreference Approach

“…2012; Janoušek et al. 2015; Liu et al. 2015) we tested for signatures of introgression within and between taxa from the M. musculus group (here, M. m. musculus and M. m. domesticus ), the M. spretus group ( M. spretus , M. spicilegus , and M. macedonicus ), and between M. cervicolor , M. cookii , and M. caroli .…”

A performance study of the impact of recombination on species tree analysis

“…Our empirical study utilized genomic sequence data from a previous phylogenomic study of house mouse and sister species [28]. The dataset contains SNPs sampled broadly from 19 chromosomes which were genotyped using the Mouse Diversity Array [29].…”

“…We used phased haploid sequences from 58 samples representing 8 different mouse species. (See [28] for details about genotyping and phasing. )…”

Bayesian Inference Of Phylogenetic Networks From Bi-allelic Genetic Markers

“…Horizontal gene transfer is ubiquitous in 71 prokaryotes [9,10], and several bodies of work are pointing to much larger extent and 72 role of hybridization in eukaryotic evolution than once thought [8,[11][12][13][14][15]. Not only does 73 hybridization play an important role in the genomic diversification of several eukaryotic 74 groups, but increasing evidence is pointing to the adaptive role it has played, for 75 example, in wild sunflowers [16], humans [17], macaques [18], mice [19], butterflies [20], 76 and mosquitoes [21,22].…”