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

Ahmad Mahmoudihttp://orcid.org/https://orcid.org/0000-0003-4698-137X 1 , 2 , Lutz C. Maul 3 , Masoumeh Khoshyar 4 , Jamshid Darvish 2 , 5 , Mansour Aliabadian 2 , 6  and Boris Kryštufek 7
  • 1 Department of Epidemiology and Biostatistics, Pasteur Institute of Iran, Pasteur Str., Tehran 1316943551, Iran
  • 2 Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • 3 Senckenberg Research Institute, Research Station of Quaternary Palaeontology Weimar, Am Jakobskirchhof 4, 99423 Weimar, Germany
  • 4 Department of Geology, Faculty of Sciences, University of Zanjan, Zanjan, Iran
  • 5 Rodentology Research Department, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • 6 Zoological Innovations Research Department, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • 7 Slovenian Museum of Natural History, Prešernova 20, Ljubljana, Slovenia
Ahmad MahmoudiORCID iD: https://orcid.org/0000-0003-4698-137X
  • Corresponding author
  • Department of Epidemiology and Biostatistics, Pasteur Institute of Iran, Pasteur Str., Tehran 1316943551, Iran
  • Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • orcid.org/0000-0003-4698-137X
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, Lutz C. Maul
  • Senckenberg Research Institute, Research Station of Quaternary Palaeontology Weimar, Am Jakobskirchhof 4, 99423 Weimar, Germany
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, Masoumeh Khoshyar, Jamshid Darvish
  • Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • Rodentology Research Department, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
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, Mansour Aliabadian
  • Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
  • Zoological Innovations Research Department, Institute of Applied Zoology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
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and Boris Kryštufek

Abstract

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 km2, making it one of the largest among arvicolines.

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Mammalia is a peer-reviewed journal devoted to the inventory, analysis and interpretation of Mammalian diversity. It publishes original results on all aspects of systematics (comparative, functional and evolutionary morphology; morphometrics; phylogeny; biogeography; taxonomy and nomenclature), biology, ecology and conservation of mammals.

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