Origin and radiation of the house mouse: mitochondrial DNA phylogeny

Abstract

On the basis of patterns of allele frequency variation in nuclear genes (Din et al., in press) it has been proposed that the house mouse M. musculus originated in the northern Indian subcontinent, from where it radiated in several directions to form the well-described peripheral subspecies (M. m. domesticus, M. m. ~~lusculu.s and M. MZ. custuneus). Here we use a mitochondrial DNA (mtDNA) phylogeny to test this hypothesis and to analyse the historical and demographic events that have accompanied this differentiation. This marker also provides a powerful means to check for genetic continuity between the central and peripheral populations. We studied restriction site polymorphism of samples from India and the Middle East as well as samples from the rest of Eurasia and northern Africa. M. m. domesticus and M. m. muscdus are both monophyletic for mtDNA and belong to the subspecies-specific mtDNA lineages that have been described previously. Average nucleotide diversity is low in M. 112. mu,r~ulu.s (0,2L5%). It is not only higher in M. m. domesticus (0.7-0.9%) but the distribution of pairwise divergence is wider, and the rate of evolution in this branch appears to be higher than in M. m. mus~u/us. The nucleotide diversity found in M. m. castaneus (0.4%) is due to the existence of two rather divergent linages with little intralineage variation. These two lineages are part of a diversified bush of the phylogenetic tree that also comprises several previously undescribed branches and includes all samples from the northern Indian subcontinent and Iran. The degree of diversity found in each of the samples from this region is high (1.2Z2.4%) although they come from small geographic areas. This agrees well with the idea that the origin of the radiation was in the northern Indian subcontinent. However, as neither haplotypcs on the M. MI. r1on~c.vtia1.v nor on the M. 171. ~~~cr.sc~ulus branches were found in this region, there appear to be important phylogeographic discontinuities between this central region and these periphcrial subspecies. On the basis of the present results and the nuclear data (Din et al., in press), we propose that M. n~u.cc~u1zr.s originated in the north of the Indian subcontinent. Our calibration of the evolutionary rate of mtDNA in mice suggests that the mouse settlement in this region could be as old as 900 000 years. Possibly from there, a first radiation could have reached the Middle East and the Caspian Sea, where the M. 1~. ~lot~~~stic~~~.s and M. tw. t~~u.s~~du.s lineages, respectively, would have started to difrcrentiate a few hundred thousand years ago, and from where they could have coloniscd the peripheral part of their ranges only recently. M. MI. c~ostmcus appears from its mtDNA to be a recent offshoot of the northern Indian population. This multiple and gradual radiation ultimately led to recent peripheral secondary contacts, such as the well-known European hybrid zone.

Signatures of Reproductive Isolation in Patterns of Single Nucleotide Diversity Across Inbred Strains of Mice

“…This observation suggests that the hybrid zone is maintained by a balance between selection against hybrids and dispersal (Barton and Gale 1993). Secondary contact between M. domesticus and M. musculus has occurred recently (5000-10,000 years ago; Auffray et al 1990) relative to estimates of divergence time (500,000 years ago; Boursot et al 1996;Din et al 1996), consistent with the accumulation of reproductive isolation in allopatry according to a Dobzhansky-Muller model.…”

Genetic Dissection of a Key Reproductive Barrier Between Nascent Species of House Mice

“…Three recognizable subspecies diverged from a common ancestor only 500,000 generations ago (She et al 1990;Boursot et al 1996;Suzuki et al 2004;Salcedo et al 2007;Geraldes et al 2008). Despite this short divergence time, several lines of evidence indicate reproductive isolation between two of the subspecies, Mus musculus musculus and Mus musculus domesticus.…”

Reproductive Isolation in Hybrid Mice Due to Spermatogenesis Defects at Three Meiotic Stages

“…Two subspecies of mouse, Mus musculus domesticus and M. m. musculus, diverged from their common ancestor 0.3-1.0 MYA (Yonekawa et al 1980;Moriwaki 1994;Bonhomme and Guénet 1996;Boursot et al 1996;Din et al 1996). M. m. domesticus ranges across western Europe and the Middle East, whereas M. m. musculus ranges throughout eastern Europe and northern Asia (Bonhomme and Guénet 1996).…”