Isolation and gene flow: inferring the speciation history of European house mice

Abstract

Inferring the history of isolation and gene flow during species differentiation can inform us on the processes underlying their formation. Following their recent expansion in Europe, two subspecies of the house mouse (Mus musculus domesticus and Mus musculus musculus) have formed a hybrid zone maintained by hybrid incompatibilities and possibly behavioural reinforcement, offering a good model of incipient speciation. We reconstruct the history of their divergence using an approximate Bayesian computation framework and sequence variation at 57 autosomal loci. We find support for a long isolation period preceding the advent of gene flow around 200,000 generations ago, much before the formation of the European hybrid zone a few thousand years ago. The duration of the allopatric episode appears long enough (74% of divergence time) to explain the accumulation of many post-zygotic incompatibilities expressed in the present hybrid zone. The ancient contact inferred could have played a role in mating behaviour divergence and laid the ground for further reinforcement. We suggest that both subspecies originally colonized the Middle East from the northern Indian subcontinent, domesticus settling on the shores of the Persian Gulf and musculus on those of the Caspian Sea. Range expansions during interglacials would have induced secondary contacts, presumably in Iran, where they must have also interacted with Mus musculus castaneus. Future studies should incorporate this possibility, and we point to Iran and its surroundings as a hot spot for house mouse diversity and speciation studies.

The Pace of Hybrid Incompatibility Evolution in House Mice

“…In line with the original model (Orr 1995), our test of the snowball effect assumes that gene flow between subspecies ceased after their initial divergence (Wang et al 2013). This assumption appears to be violated in house mice, although estimated levels of historical gene flow are low (Duvaux et al 2011;Geraldes et al 2011), with a potential increase in the hybridization rate very recently (Pool and Nielsen 2009). The potential impact of gene flow on our results is not easy to predict.…”

“…High levels of gene flow would likely erase the snowball signature. However, historical levels of gene flow between house mouse subspecies appear to have been relatively low (Duvaux et al 2011;Geraldes et al 2011), an inference supported by the phylogenetic history observed across the subspecies' genomes (Keane et al 2011).…”

“…House mice (Mus musculus) are a model system for understanding the genetics of speciation and feature an expansive genetic and genomic toolkit. The three subspecies diverged recently (Geraldes et al 2008(Geraldes et al , 2011White et al 2009;Duvaux et al 2011), perhaps ,350,000 years ago (Geraldes et al 2011). Two pairs of subspecies show partial reproductive isolation, particularly in the form of hybrid male sterility (Forejt and Iványi 1974;Britton-Davidian et al 2005;Vyskočilová et al 2005;Good et al 2008a;White et al 2012a), indicating speciation is in progress.…”

“…Two pairs of subspecies show partial reproductive isolation, particularly in the form of hybrid male sterility (Forejt and Iványi 1974;Britton-Davidian et al 2005;Vyskočilová et al 2005;Good et al 2008a;White et al 2012a), indicating speciation is in progress. House mouse subspecies also hybridize in the wild (Boursot et al 1993;Sage et al 1993;Duvaux et al 2011;Jing et al 2014), providing opportunities to connect the genetics of reproductive isolation phenotypes in the laboratory with gene flow in nature. The existence of gene flow violates the assumption of complete allopatry after divergence used in the snowball model.…”

Genetics and Evolution of Hybrid Male Sterility in House Mice

“…In natural populations, hybridization has occurred between the two subspecies in human-mediated zones of secondary contact (Orth et al 1998). Hybridization may have also occurred in Iran during subspecies range expansion (Duvaux et al 2011). Patterns of genetic differentiation indicate higher levels of introgression from M. m. domesticus into M. m. castaneus than between M. m. musculus and M. m. domesticus (Geraldes et al 2008(Geraldes et al , 2011.…”