Further resolution of the house mouse (Mus musculus) phylogeny by integration over isolation-with-migration histories

Abstract

Background: The three main subspecies of house mice, Mus musculus castaneus, Mus musculus domesticus, and Mus musculus musculus, are estimated to have diverged ~ 350-500KYA. Resolution of the details of their evolutionary history is complicated by their relatively recent divergence, ongoing gene flow among the subspecies, and complex demographic histories. Previous studies have been limited to some extent by the number of loci surveyed and/or by the scope of the method used. Here, we apply a method (IMa3) that provides an estimate of a population phylogeny while allowing for complex histories of gene exchange.

Results: Results strongly support a topology with M. m. domesticus as sister to M. m. castaneus and M. m. musculus. In addition, we find evidence of gene flow between all pairs of subspecies, but that gene flow is most restricted from M. m. musculus into M. m. domesticus. Estimates of other key parameters are dependent on assumptions regarding generation time and mutation rate in house mice. Nevertheless, our results support previous findings that the effective population size, N_e, of M. m. castaneus is larger than that of the other two subspecies, that the three subspecies began diverging ~ 130 - 420KYA, and that the time between divergence events was short.

Conclusions: Joint demographic and phylogenetic analyses of genomic data provide a clearer picture of the history of divergence in house mice.

Keywords: Divergence; IMa3; Population size; Speciation.

Fig. 1

Representations of estimated IM models generated by IMa3 and the IMfig program [37] for the three subspecies of house mouse. The phylogeny is depicted as a series of boxes organized hierarchically, with ancestor boxes positioned in between the corresponding descendants, and the width of boxes proportional to estimated N_e. Gray arrows extending to the left and right of the right boundary of each population box depict 95% confidence intervals for N_e values. Splitting times are depicted as solid horizontal lines, with text values on the left. Confidence intervals for splitting times are shown as vertical gray arrows on the left, and parallel dashed lines. Migration arrows (if shown) indicate estimated 2 Nm values from one population to another over the time interval when both populations exist. Arrows are shown only for estimated migration rates that are statistically significant at or above the 0.05 level (^*p < 0.05, ^**p < 0.01, ^***p < 0.001 [33]). (a) without a ghost population (b) with a ghost population included. Estimates assume 1.5 generations/year and 6 × 10⁻⁹ mutations per base pair per generation

Fig. 2

A representation of an estimated IM model generated by IMa3 and the IMfig program [37] for house mice using six nuclear loci from Geraldes et al. [27]. Details are as given in Fig. 1. Estimates assume 1.5 generations/year and 6 × 10⁻⁹ mutations per base pair per generation