Inferring the history of speciation in house mice from autosomal, X‐linked, Y‐linked and mitochondrial genes

Abstract

Patterns of genetic differentiation among taxa at early stages of divergence provide an opportunity to make inferences about the history of speciation. Here, we conduct a survey of DNA-sequence polymorphism and divergence at loci on the autosomes, X chromosome, Y chromosome and mitochondrial DNA in samples of Mus domesticus, M. musculus and M. castaneus. We analyzed our data under a divergence with gene flow model and estimate that the effective population size of M. castaneus is 200 000–400 000, of M. domesticus is 100 000–200 000 and of M. musculus is 60 000–120 000. These data also suggest that these species started to diverge approximately 500 000 years ago. Consistent with this recent divergence, we observed considerable variation in the genealogical patterns among loci. For some loci, all alleles within each species formed a monophyletic group, while at other loci, species were intermingled on the phylogeny of alleles. This intermingling probably reflects both incomplete lineage sorting and gene flow after divergence. Likelihood ratio tests rejected a strict allopatric model with no gene flow in comparisons between each pair of species. Gene flow was asymmetric: no gene flow was detected into M. domesticus, while significant gene flow was detected into both M. castaneus and M. musculus. Finally, most of the gene flow occurred at autosomal loci, resulting in a significantly higher ratio of fixed differences to polymorphisms at the X and Y chromosomes relative to autosomes in some comparisons, or just the X chromosome in others, emphasizing the important role of the sex chromosomes in general and the X chromosome in particular in speciation.

Chromosomal dynamics of nucleolar organizer regions (NORs) in the house mouse: micro-evolutionary insights

“…This result agrees with increasing evidence of a southeast Asian lineage within MUS, as well as current views of the geographic origin of the MUS genomic contribution to MOL (Yonekawa et al, 2012). NOR variability levels are in agreement with colonization patterns that predict higher diversity in populations from the area of origin compared with those present in peripheral regions (Geraldes et al, 2008;Rajabi-Maham et al, 2008). Thus, CAS from the Indo-Pakistani region has the highest mean heterozygosity value among the subspecies (Table 1), although MOL is the one that shows the highest diversity in number of NOR-bearing chromosomes (13 vs 11 in the other subspecies).…”

“…The NOR-based phylogeny is essentially compatible with the currently established relationships for the three main subspecies: DOM is the most differentiated subspecies whereas MUS and CAS are more closely related (Bonhomme et al, 2007), although all sister group associations have been found depending on the marker used (see Bonhomme et al, 2007;Geraldes et al, 2008). MOL, which carries a MUS/CAS composite genome has, as expected, an intermediate position in the tree.…”

“…From its native Eurasian distribution, the house mouse subsequently expanded its range worldwide through passive transport with humans. The evolutionary history of the subspecific radiation of M. musculus has been extensively documented and most of the molecular analyses concur with the paleontological data in identifying the Indian subcontinent as the cradle from which the species expanded (Bonhomme et al, 2007;Geraldes et al, 2008;Duvaux et al, in press). This region is currently occupied by M. m. castaneus and represents the ancestral range of the species.…”

“…This extensive NOR diversity indicated that high rates of inter-chromosomal transposition existed within the Mus genome in the absence of cytogenetically visible rearrangements. The house mouse is an Eurasian polytypic species with five currently recognized subspecies: M. m. domesticus, the Western European house mouse, occupies western Europe and the Mediterranean Basin to southwestern Iran; M. m. musculus, the eastern European house mouse, extends in fact from northern Europe to China; M. m. castaneus, the Asian house mouse, is present from central to southeast Asia (Bonhomme et al, 2007;Geraldes et al, 2008;Rajabi-Maham et al, 2008); M. m. molossinus, the Japanese house mouse, is restricted to Japan and neighboring countries and originated by hybridization between M. m. musculus and M. m. castaneus (Yonekawa et al, 2012); finally M. m. gentilulus, the Arabian house mouse, is the most recently rehabilitated subspecies occupying the southern Arabian peninsula (Prager et al, 1998;Duplantier et al, 2002). Two extant hybrid zones exist involving M. m. musculus, one with M. m. domesticus in Europe and the other with M. m. castaneus in China (Bonhomme et al, 2007).…”

“…This region is currently occupied by M. m. castaneus and represents the ancestral range of the species. Analyses based on mitochondrial or sex-linked sequences generally define monophyletic subspecific lineages, particularly in the peripheral populations of the subspecies, that is, Europe, Arabia, Japan and Southeast Asia (Prager et al, 1998;Duplantier et al, 2002;Geraldes et al, 2008;RajabiMaham et al, 2008). In contrast, the fewer studies using autosomal nuclear markers have highlighted the genetic interrelatedness of the subspecies gene pools due to an ancient episode of gene flow or to lineage sorting (Bonhomme et al, 2007;Geraldes et al, 2008;Duvaux et al, in press).…”