Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA

Abstract

We examined the sequence variation of mitochondrial DNA control region and cytochrome b gene of the house mouse (Mus musculus sensu lato) drawn from ca. 200 localities, with 286 new samples drawn primarily from previously unsampled portions of their Eurasian distribution and with the objective of further clarifying evolutionary episodes of this species before and after the onset of human-mediated long-distance dispersals. Phylogenetic analysis of the expanded data detected five equally distinct clades, with geographic ranges of northern Eurasia (musculus, MUS), India and Southeast Asia (castaneus, CAS), Nepal (unspecified, NEP), western Europe (domesticus, DOM) and Yemen (gentilulus). Our results confirm previous suggestions of Southwestern Asia as the likely place of origin of M. musculus and the region of Iran, Afghanistan, Pakistan, and northern India, specifically as the ancestral homeland of CAS. The divergence of the subspecies lineages and of internal sublineage differentiation within CAS were estimated to be 0.37-0.47 and 0.14-0.23 million years ago (mya), respectively, assuming a split of M. musculus and Mus spretus at 1.7 mya. Of the four CAS sublineages detected, only one extends to eastern parts of India, Southeast Asia, Indonesia, Philippines, South China, Northeast China, Primorye, Sakhalin and Japan, implying a dramatic range expansion of CAS out of its homeland during an evolutionary short time, perhaps associated with the spread of agricultural practices. Multiple and non-coincident eastward dispersal events of MUS sublineages to distant geographic areas, such as northern China, Russia and Korea, are inferred, with the possibility of several different routes.

Historical Introduction of Japanese Wild Mice, Mus musculus, from South China and the Korean Peninsula

“…, Hitoshi Suzuki 1, * , Kazuo Moriwaki except for CAS-1, which appears to have spread rapidly during prehistoric times from a source region somewhere in India to the far eastern periphery of the CAS territory, including South China and Japan (Suzuki et al, 2013). Notably, the CAS-1 sublineage has low nucleotide diversity, which is consistent with the recent phylogeographic work on the castaneus subspecies group by Rajabi-Maham et al (2012); see also Bonhomme and Searle (2012).…”

“…The presence of the subgroups is suggestive of a stepwise historical range expansion of CAS-1. The expansion time of the Cytb haplotypes, at a relatively higher mutation rate (e.g., 8.5% per million years per lineage), was roughly estimated to be 9,000 and 4,500 years ago for CAS-1 and CAS-1a, respectively (Suzuki et al, 2013;Kuwayama et al, unpublished) (Fig. 1B).…”

“…There is good evidence for domestication of cereal crops, including rice and millet, by about 9,000 years ago in South and East Asia (Khush, 1997;Londo et al, 2006;Liu et al, 2007;Molina et al, 2011). Thus, the CAS-1 range expansion may be associated with the spread of cereal cultivation in these regions (Suzuki et al, 2013). With regard to the CAS-1a group expansion, it is of interest to note recent molecular and archaeological evidence for the origin of cultivated rice (Fuller et al, 2010(Fuller et al, , 2011Huang et al, 2012).…”

“…The MUS lineage consists of two sublineages, major (MUS-1) and minor (MUS-2) groups, which cover a broad range of North China and Russia, with an estimated divergence time of 150,000 years ago (Suzuki et al, 2013). Cytb sequence analyses have provided evidence for rapid population expansion of MUS-1, with an estimated time of 26,000 years ago at a mutation rate of 8.5% per million years per lineage (Suzuki et al, 2013) (Fig. 1B).…”

“…However, the exact geographic origins of Japanese wild mice are uncertain due to the veiled histories of subspecies groups in East Asia. From our recent phylogeographic work on mice collected over wide areas of the two subspecies groups (Nunome et al, 2010;Suzuki and Aplin, 2012;Suzuki et al, 2013), it is now possible to more accurately pinpoint the multiple places of origin of Japanese mice in the Korean Peninsula and South China. Here we describe recent achievements related to this issue and discuss the possible interpretation of the historical migrations of wild mice from continental areas to Japan.…”