Skip to main content
SpringerLink
Log in

A Biogeographic View of Apodemus in Asia and Europe Inferred From Nuclear and Mitochondrial Gene Sequences

  • Published:
Biochemical Genetics Aims and scope Submit manuscript

Abstract

Sequences of the mitochondrial cyt b gene and nuclear IRBP, RAGI, I7, and vWF genes were used to assess the evolutionary history of major lineages of Apodemus, in particular to better understand dispersal between Asia and Europe. Our data show eight extant lineages of Late Tertiary origin: Apodemus agrarius, A. semotus, A. peninsulae, A. speciosus, A. argenteus, A. gurkha, A. mystacinus, and A. sylvaticus. Monophyly of two European lineages (A. mystacinus and A. sylvaticus) and four Asian lineages (A. agrarius, A. semotus, A. peninsulae, and A. speciosus) was confirmed with high bootstrap support. Together with literature data, the available molecular data depict three crucial evolutionary events: (1) initial wide dispersal and subsequent radiation around 6 million years ago, (2) region-specific radiations in Europe and southern China around 2 million years ago, and (3) westward dispersal of A. agrarius to Europe in the Late Quaternary.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adler GH (1995) Habitat relations within lowland grassland rodent communities in Taiwan. J Zool 237:563–576

    Article  Google Scholar 

  • Adler GH (1996) Habitat relations of two endemic species of highland forest rodents in Taiwan. Zool Stud 35:105–110

    Google Scholar 

  • Bellinvia E (2004) A phylogenetic study of the genus Apodemus by sequencing the mitochondrial DNA control region. J Zool Syst Evol Res 42:289–297

    Article  Google Scholar 

  • Bryja J, Rehák Z (1998) Community of small terrestrial mammals (Insectivora, Rodentia) in dominant habitats of the Protected Landscape Area of Poodøí (Czech Republic). Folia Zool 47:249–260

    Google Scholar 

  • Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell 65:175–187

    Article  PubMed  CAS  Google Scholar 

  • Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158

    Article  CAS  Google Scholar 

  • Chelomina GN, Suzuki H (2006) Molecular evolution and phylogeography of west-Palaearctic wood mice of the genus Sylvaemus based on the data on variation of nuclear (IRBP) and mitochondrial (cyt b) DNA genes. Zool Zhurnal 85:219–234

    Google Scholar 

  • Chelomina GN, Suzuki H, Tsuchiya K, Moriwaki K, Lyapunova EA, Vorontsov NN (1998) Sequencing of the mtDNA cytochrome b gene and reconstruction of the maternal relationships of wood and field mice of the genus Apodemus (Muridae, Rodentia). Russian J Genet 34:529–539

    CAS  Google Scholar 

  • Chinen AA, Suzuki H, Aplin KP, Tsuchiya K, Suzuki S (2005) Preliminary genetic characterization of two lineages of black rats (Rattus rattus sensu lato) in Japan, with evidence for introgression at several localities. Genes Genet Syst 80:367–375

    Article  PubMed  CAS  Google Scholar 

  • Conroy CJ, Cook JA (1999) MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. J Mamm Evol 6:221–245

    Article  Google Scholar 

  • Corbet GB (1978) The mammals of the Palaearctic Region: a taxonomic review. British Museum (Natural History) and Cornell University Press, London and Ithaca

    Google Scholar 

  • Corbet GB, Hill JE (1992) The mammals of the Indomalayan Region: a systematic review. Oxford University Press, London, 488 pp

    Google Scholar 

  • Felsenstein J (1993) Phylip (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle

  • Filippucci MG (1992) Allozyme variation and divergence among European, Middle Eastern, and North African species of the genus Apodemus (Rodentia, Muridae). Isr J Zool 38:193–218

    Google Scholar 

  • Filippucci MG, Simson S, Nevo E (1989) Evolutionary biology of the genus Apodemus Kaup, 1829 in Israel: allozymic and biometric analyses with description of a new species: Apodemus hermonensis (Rodentia, Muridae). Boll Zool 56:361–376

    Google Scholar 

  • Filippucci MG, Storch G, Macholán M (1996) Taxonomy of the genus Sylvaemus in western Anatolia: morphological and electrophoretic evidence (Mammalia: Rodentia: Muridae). Senckenb Biol 75:1–14

    Google Scholar 

  • Filippucci MG, Macholán M, Michaux JR (2002) Genetic variation and evolution in the genus Apodemus (Muridae: Rodentia). Biol J Linn Soc 75:395–419

    Google Scholar 

  • Han S-H, Wakana S, Suzuki H, Hirai Y, Tsuchiya K (1996) Variation of the mitochondrial DNA and the nuclear ribosomal DNA in the striped field mouse Apodemus agrarius on the mainland and offshore islands of South Korea. Mammal Study 21:125–136

    Article  Google Scholar 

  • Hille A, Tarkhnishvili D, Meinig H, Hutterer R (2002) Morphometric, biochemical and molecular traits in Caucasian wood mice (Apodemus/Sylvaemus), with remarks on species divergence. Acta Theriol 47:389–416

    Google Scholar 

  • Huchon D, Catzeflis FM, Douzery EJP (1999) Molecular evolution of the nuclear von Willebrand Factor gene in mammals and the phylogeny of rodents. Mol Biol Evol 16:577–589

    PubMed  CAS  Google Scholar 

  • Huchon D, Madsen O, Sibbald MJJB, Ament K, Stanhope MJ, Catzeflis F, de Jong WW, Douzery EJP (2002) Rodent phylogeny and a timescale for the evolution of glires: evidence from an extensive taxon sampling using three nuclear genes. Mol Biol Evol 19:1053–1065

    PubMed  CAS  Google Scholar 

  • Jansa SA, Voss RS (2000) Phylogenetic studies on didelphid marsupials I. Introduction and preliminary results from nuclear IRBP gene sequences. J Mammal Evol 7:43–77

    Article  Google Scholar 

  • Jansa SA, Goodman SM, Tucker PK (1999) Molecular phylogeny and biogeography of Madagascar’s native rodents (Muridae: Nesomyinae): a test of the single origin hypothesis. Cladistics 15:253–270

    Article  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  PubMed  CAS  Google Scholar 

  • Kostenko VA (2000) Rodents (Rodentia) of the Russian Far East. Institute of Biology and Soil Sciences, Russian Academy of Sciences, Far East Branch, Dalnauka, Vladivostok, 210 pp (in Russia)

    Google Scholar 

  • Krautwurst D, Yau KW, Reed RR (1998) Identification of ligands for olfactory receptors by functional expression of a receptor library. Cell 95:917–926

    Article  PubMed  CAS  Google Scholar 

  • Krystufek B (1985) Variability of Apodemus agrarius (Pallas, 1771) (Rodentia, Mammalia) in Yugoslavia and some data on its distribution in the northwestern part of the country. Bioloski Vestnik 33:27–40

    Google Scholar 

  • Liu W, Wei F, Li M, Jiang X, Feng Z, Hu J (2004) Molecular phylogeny and taxonomy of wood mice (genus Apodemus Kaup, 1829) based on complete mtDNA cytochrome b sequences, with emphasis on Chinese species. Mol Phylogenet Evol 33:1–15

    Article  PubMed  CAS  Google Scholar 

  • Macholán M, Filippucci MG, Benda P, Frynta D, Sadlova J (2001) Allozyme variation and systematics of the genus Apodemus (Muridae: Rodentia) in Asia Minor and Iran. J Mammal 82:799–813

    Article  Google Scholar 

  • Mancuso DJ, Tuley EA, Westfield LA, Worrall NK, Shelton-Inloes BB, Sorace JM, Alevy YG, Sadler JE (1989) Structure of the gene for human von Willebrand factor. J Biol Chem 264:19514–19527

    PubMed  CAS  Google Scholar 

  • Martin Y, Gerlach G, Schloetterer C, Meyer A (2000) Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol Phylogenet Evol 16:37–47

    Article  PubMed  CAS  Google Scholar 

  • May-Collado LJ, Agnarsson I (2006) Cytochrome b and Bayesian inference of whale phylogeny. Mol Phylogenet Evol 38:344–354

    Article  PubMed  CAS  Google Scholar 

  • McShea WJ, Pagels J, Orrock J, Harper E, Koy K (2003) Mesic deciduous forest as patches of small-mammal richness within an Appalachian Mountain Forest. J Mammal 84:627–643

    Article  Google Scholar 

  • Mezhzherin SV, Mikhailenko AG (1991) On the species identity of Apodemus sylvaticus tscherga (Rodentia, Muridae) of the Altai Mts. Vestnik Zoologii 1991:35–44 (in Russian with English summary)

    Google Scholar 

  • Michaux JR, Chevret P, Filippucci MG, Macholán M (2002) Phylogeny of the genus Apodemus with a special emphasis to the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol 23:123–136

    Article  PubMed  CAS  Google Scholar 

  • Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R (2003) Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Mol Ecol 12:685–697

    Article  PubMed  CAS  Google Scholar 

  • Michaux JR, Libois R, Paradis E, Filippucci MG (2004) Phylogeographic history of the yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Mol Phylogenet Evol 32:788–798

    Article  PubMed  CAS  Google Scholar 

  • Michaux JR, Bellinvia E, Lymberakis P (2005) Taxonomy, evolutionary history and biogeography of the broad-toothed field mouse (Apodemus mystacinus) in the eastern Mediterranean area based on mitochondrial and nuclear genes. Biol J Linn Soc 85:53–63

    Article  Google Scholar 

  • Millien V (2004) Relative effects of climate change, isolation and competition on body-size evolution in the Japanese field mouse, Apodemus argenteus. J Biogeogr 31:1267–1276

    Article  Google Scholar 

  • Musser GG, Carleton MD (1993) Family muridae. In: Wilson DE, Reeder DM (eds) Mammal species of the world, 2nd edn. Smithsonian Institution Press, Washington and London, pp 501–755

    Google Scholar 

  • Musser GG, Carleton MD (2005) Family muridae. In: Wilson DE, Reeder DM (eds) Mammal species of the world, 3rd edn. Johns Hopkins University Press, Baltimore, pp 894–1531

    Google Scholar 

  • Musser GG, Brothers EM, Carleton MD, Hutterer R (1996) Taxonomy and distributional records of Oriental and European Apodemus, with a review of the Apodemus-Sylvaemus problem. Bonner Zool Beitr 46:143–190

    Google Scholar 

  • Orlov VN, Bulatova NS, Nadjafova RS, Kozlovsky AI (1996) Evolutionary classification of European wood mice of the subgenus Sylvaemus based on allozyme and chromosome data. Bonner Zool Beitr 46:191–202

    Google Scholar 

  • Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of the AIC and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Reutter BA, Petit E, Bruenner H, Vogel P (2003) Cytochrome b haplotype divergences in West European Apodemus. Mammal Biol 68:153–164

    Article  Google Scholar 

  • Rietschel S, Storch G (1974) Außgewöhlich erhaltene Waldmäuse (Apodemus atavus Heller, 1936) aus dem ober-Pliozän von Willerhausen am Harz. Senkenberg Lethaea 54:491–519

    Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rutschmann F (2005) Bayesian molecular dating using PAML/multidivtime: a step-by-step manual. University of Zurich, Switzerland. http://www.plant.ch

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sato JJ, Suzuki H (2004) Phylogenetic relationships and divergence times of the genus Tokudaia within Murinae (Muridae; Rodentia) inferred from the nucleotide sequences encoding the mitochondrial cytochrome b gene and nuclear recombination-activating gene 1 and interphotoreceptor retinoid-binding protein. Can J Zool 82:1343–1351

    Article  CAS  Google Scholar 

  • Sato JJ, Hosoda T, Wolsan M, Suzuki H (2004) Molecular phylogeny of arctoids (Mammalia: Carnivora) with emphasis on phylogenetic and taxonomic positions of the ferret-badgers and skunks. Zool Sci 21:111–118

    Article  PubMed  CAS  Google Scholar 

  • Sekijima T, Sone K (1994) Role of interspecific competition in the coexistence of Apodemus argenteus and A. speciosus (Rodentia, Muridae). Ecol Res 9:237–244

    Article  Google Scholar 

  • Serizawa K, Suzuki H, Tsuchiya K (2000) A phylogenetic view on species radiation in Apodemus inferred from variation of nuclear and mitochondrial genes. Biochem Genet 38:27–40

    Article  PubMed  CAS  Google Scholar 

  • Shimada T (2001) Hoarding behaviors of two wood mouse species: different preference for acorns of two Fagaceae species. Ecol Res 16:127–133

    Article  Google Scholar 

  • Springer MS, Burk A, Kavanagh JR, Waddell VG, Stanhope MJ (1997) The interphotoreceptor retinoid binding protein gene in therian mammals: implications for higher level relationships and evidence for loss of function in the marsupial mole. Proc Natl Acad Sci USA 94:13754–13759

    Article  PubMed  CAS  Google Scholar 

  • Stanhope MJ, Czelusniak J, Si J-S, Nickerson J, Goodman M (1992) A molecular perspective on mammalian evolution from the gene encoding interphotoreceptor retinoid binding protein, with convincing evidence for bat monophyly. Mol Phylogenet Evol 1:148–160

    Article  PubMed  CAS  Google Scholar 

  • Stanhope MJ, Smith MR, Waddell VG, Porter CA, Shivji MS, Goodman M (1996) Mammalian evolution and the interphotoreceptor retinoid binding protein (IRBP) gene: convincing evidence for several superordinal clades. J Mol Evol 43:83–92

    Article  PubMed  CAS  Google Scholar 

  • Storch G (1975) Eine Mittelpleistozäne Nager-Fauna von der Insel Chios, Ägäis (Mammalia, Rodentia). Senckenb Biol 56:165–189

    Google Scholar 

  • Storch G (1977) Die Ausbreitung der Felsenmaus (Apodemus mystacinus): zur Problematik der Inselbesiedlung und tiergeographie der Ägäis. Natur Mus 107:174–182

    Google Scholar 

  • Suzuki H, Tsuchiya K, Sakaizumi M, Wakana S, Sakurai S (1994) Evolution of restriction sites of ribosomal DNA in natural populations of the field mouse, Apodemus speciosus. J Mol Evol 38:107–112

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, Tsuchiya K, Takezaki N (2000) A molecular phylogenetic framework for the Ryukyu endemic rodents Tokudaia osimensis and Diplothrix legata (Rodentia, Mammalia). Mol Phylogenet Evol 15:15–24

    Article  PubMed  CAS  Google Scholar 

  • Suzuki H, Sato JJ, Tsuchiya K, Luo J, Zhang Y-P, Wang Y-X, Jiang X-L (2003) Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biol J Linn Soc 80:469–481

    Article  Google Scholar 

  • Suzuki H, Shimada T, Terashima M, Tsuchiya K, Aplin K (2004) Temporal, spatial, and ecological modes of evolution of Eurasian Mus based on mitochondrial and nuclear gene sequences. Mol Phylogenet Evol 33:626–646

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2003) PAUP: phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657

    PubMed  CAS  Google Scholar 

  • Vorontsov NN, Boyeskorov GG, Mezhzherin SV, Lyapunova EA, Kandaurov AS (1992) Systematics of the Caucasian wood mice of the subgenus Sylvaemus (Mammalia, Rodentia, Apodemus). Zool Zh 71:119–131 (in Russian with English summary)

    Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

  • Yang Z, Yoder AD (2003) Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Syst Biol 52:705–716

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are most grateful to K. Tsuchiya and K. Moriwaki for their encouragement and to R. Nakayama for technical support. We also thank J. Luo, Y.-P. Zhang, Y.-X. Wang, X.-L. Jiang, P. Vogel, and S.-H. Han for valuable suggestions. This study was supported in part by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

Author information

Authors and Affiliations

  1. Graduate School of Environmental Earth Science, Hokkaido University, Sapporo, 060-0810, Japan

    Hitoshi Suzuki & Keiko Serizawa

  2. Department of Biology, University of Rome “Tor Vergata”, 00133, Rome, Italy

    Maria Grazia Filippucci

  3. Institute of Biology and Soil Science, Russian Academy of Sciences Far East Branch, Vladivostok, 690022, Russia

    Galina N. Chelomina

  4. Faculty of Life Science and Technology, Fukuyama University, Higashimura-cho, Aza, Sanzo, 985, Fukuyama, 729-0292, Japan

    Jun J. Sato

  5. Institute of Evolution, University of Haifa, Mount Carmel, Haifa, 31905, Israel

    Eviatar Nevo

Authors
  1. Hitoshi Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria Grazia Filippucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Galina N. Chelomina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jun J. Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Keiko Serizawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eviatar Nevo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hitoshi Suzuki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Suzuki, H., Filippucci, M.G., Chelomina, G.N. et al. A Biogeographic View of Apodemus in Asia and Europe Inferred From Nuclear and Mitochondrial Gene Sequences. Biochem Genet 46, 329–346 (2008). https://doi.org/10.1007/s10528-008-9149-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-008-9149-7

Keywords

Search

Navigation