Evolutionary history of water voles revisited: confronting a new phylogenetic model from molecular data with the fossil record

Recent water voles (genus Arvicola) display a prominent morphological diversity with a strong ecotypical background but with unclear taxonomic associations. We provide a novel synthetic view on the evolutionary history and the current taxonomic richness in the genus. Our molecular reconstruction, based on a 1143-bp-long sequence of cytochrome b and a 926-bp interphotoreceptor retinoid binding protein (irbp) confirmed the monophyly of four species (amphibius, sapidus, monticola and italicus) recognized thus far, and retrieved a new deeply divergent lineage from West Iran. Genetic divergence of the Iranian lineage (>9.0%) is inside the range of interspecies distances, exceeding the interspecies divergences between the remaining Arvicola species (range, 4.3 8.7%). The oldest name available for the Iranian phylogroup is Arvicola persicus de Filippi, 1865, with the type locality in Soltaniyeh, Iran. The molecular clock suggests the divergence of A. persicus in the Early Pleistocene (2.545 Ma), and the current radiation of the remaining species between 1.535 Ma (Arvicola sapidus) and 0.671 Ma. While A. sapidus possibly evolved from Arvicola jacobaeus, a fossil ancestor to A. persicus is unknown. The aquatic life-style of Mimomys savini, a direct ancestor to some fossil Arvicola, is retained in recent stem species A. sapidus and A. persicus, while a major shift toward fossorial morphotype characterizes the terminal lineages (amphibius, italicus and monticola). We suggest that habitat-dependent morphological plasticity and positive enamel differentiation in Arvicola amphibius widened its ecological niche that might trigger a range expansion across c. 12 million km(2), making it one of the largest among arvicolines.