Taxonomic Hierarchy and Evolutionary Scenario of the Genus Group Apodemus s. l. (Muridae) of the Palearctic based of Genetic Differentiation in the cyt-b Gene
Abstract
Characters of taxonomy and evolutionary scenario based on genetic differentiation of generic groups of forest and field mice Apodemus s. l. were established by analyzing the variability of the cyt-b (cytochrome-1, cytb) gene. For this purpose, 124 sequences of Apodemus s. l. and other Palearctic Muridae genera (Mus, Micromys, Rattus) were downloaded from GenBank. The adequacy of the categories of semispecies, allospecies, species, whose genetic differentiation corresponds to GD ranges of 0.03–0.06, 0.06–0.1 and 0.1–0.15, has been proven. Within the genus Sylvaemus the following species are recognised: S. (Sylvaemus) alpicola, S. (S.) arianus (= witherbyi), S. (S.) flavicollis, S. (S.) hyrcanicus, S. (S.) ponticus, S. (S.) (superspecies) sylvaticus, S. (S.) (superspecies) uralensis, S. (Karstomys) epimelas, S. (K.) mystacinus, S. (?) rusiges: within Apodemus: A. agrarius, A. chevrieri, within Alsomys: Al. argenteus, Al. ilex, Al. latronum, Al. (superspecies) major (= peninsulae), Al. nigrus, Al. semotus, Al. speciosus. Generic taxonomy remains ambiguous, which is caused not only by different scales of differentiation of most species of Western and Eastern Palaearctic lineages, but also by the lack of information on key genus-specific characters: the number of roots on upper molars and number of mammary glands for most East Asian species.
References
Amadon, D. 1966. The superspecies concept, Systematic Zoology, 15, 246-249.
https://doi.org/10.2307/sysbio/15.3.245
Bellinvia, E., Munclinger, P., Flegr, J. 1999. Application of the RAPD technique for a study of the phylogenetic relationships among eight species of the genus Apodemus. Folia Zoologica, 48, 241-248.
Bellinvia, E. 2004. A phylogenetic study of the genus Apodemus by sequencing the mitochondrial DNA control region // Journal of Zoological Systematics and Evolutionary Research, 42, 289-297.
https://doi.org/10.1111/j.1439-0469.2004.00270.x
Chelomina, G. N., Pavlenko, M. V., Kartavtseva, I. V., Boeskorov, G. G., Lyapunova, E. A., Vorotzov, N. N. 1998. Genetic differentiation of Caucasus wood mice: comparison of isozymic, chromosomal and molecular divergence. Genetika, 34, 213-225.
Darvish, J., Mohammadi, Z., Ghorbani, F., Mahmoudi, A., Dubey, S. 2015. Phylogenetic relationships of Apodemus Kaup, 1829 (Rodentia: Muridae) species in the Eastern Mediterranean inferred from mitochondrial DNA, with emphasis on Iranian species. Journal of Mammalian Evolution, 22, 583-595.
https://doi.org/10.1007/s10914-015-9294-9
Fan, Z., Liu, S., Liu, Y., Liao, L., Zhang, X., Yue, B. 2012. Phylogeography of the South China field mouse (Apodemus draco) on the southeastern Tibetan Plateau reveals high genetic diversity and glacial refugia. PLoS One, 7(5):e38184.
https://doi.org/10.1371/journal.pone.0038184
Filippucci, M. G. , Macholan, M. , Michaux, J. R. 2002. Genetic variation and evolution in the genus Apodemus (Muridae: Rodentia). Biological Journal of the Linnean Society, 75, 395-419.
https://doi.org/10.1046/j.1095-8312.2002.00032.x
Filippucci M. G., 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). Bol. Zool. 56: 361-376.
https://doi.org/10.1080/11250008909355663
Filippucci, M. G. 1992. Allozyme variation and divergence among European, Middle Eastern and North African species of the genus Apodemus (Rodentia, Muridae). Israel Journal of Zoology, 38, 193-218.
Ge, D., Feijo, A., Cheng, J., Lu, L., Liu, R., Abramov,A.V., Xia,L., Wen, Z., Zhang,W., Shi, L., Yang, Q. 2019. Evolutionary history of field mice (Murinae: Apodemus), with emphasis on morphological variation among species in China and description of a new species. Zoological Journal of Linnaen Society, 187, 518-534.
https://doi.org/10.1093/zoolinnean/zlz032
Gilbert, A. N. 1986. Mammary number and litter size in Rodentia: the "one-half rule", 83, 4828-4830.
https://doi.org/10.1073/pnas.83.13.4828
Irwin, D. M., Kocher, T. D., Wilson, A. C. 1991. Evolution of the cytochrome b gene of mammals. Journal of Molecular Evolution, 32: 128-144.
https://doi.org/10.1007/BF02515385
Kim, H. R., Park, Y. C. 2016. Erratum to: Genetic isolation of Korean populations of Apodemus peninsulae (Rodentia: Muridae) from their neighboring populations. Genes & Genomics, 38, 319.
https://doi.org/10.1007/s13258-015-0367-1
Knitlova, M., Horaček, I. 2017. Genus Apodemus in the pleistocene of Central Europe: when did the extant taxa appear? Fossil Imprint, 73, 460-481.
https://doi.org/10.2478/if-2017-0024
Krystufek, B., Luznik, M., Buzan, E. V. 2012. Mitochondrial cytochrome b sequences resolve the taxonomy of field mice (Apodemus) in the Western Balkan refugium. Acta Theriologica, 57, 1-7.
https://doi.org/10.1007/s13364-011-0045-x
Liu, S. Y., He, K., Chen, S .D., Jin, W., Murphy, R. W., Tang, M. K., Liao, R. Li, F.J. 2018. How many species of Apodemus and Rattus occur in China? A survey based on mitochondrial cyt b and morphological analyses. Zoological Research, 39, 309-320.
https://doi.org/10.24272/j.issn.2095-8137.2018.053
Liu, X., Wei F., Li, M., Jiang, X.-L. 2004. Molecular phylogeny and taxonomy of wood mice (genus Apodemus Kaup, 1829) based on complete mtDNA cytochrome b sequences, with emphasis on Chinese species. Molecular Phylogenetics and Evolution, 33(1):1-15.
https://doi.org/10.1016/j.ympev.2004.05.011
Mallet, J. 2007. Subspecies, semispecies, superspecies. Encyclopedia of Biodiversity, 7, 45-48
https://doi.org/10.1016/B978-0-12-384719-5.00138-6
Mezhzherin, S. V. 1997. Revision of mice genus Apodemus (Rodentia, Muridae) of Nothern Eurasia. Vestnik Zoologii. 31, 29-41.
Michaux, J. R., Kinet, S., Filippucci, M. G., Libois, R., Besnard, A., Catzeflis, F. 2001. Molecular identification of three sympatric species of wood mice (Apodemus sylvaticus, A. flavicollis, A. alpicola) in Western Europe (Muridae, Rodentia). Molecular Ecology Notes, 1, 260-263.
https://doi.org/10.1046/j.1471-8278.2001.00100.x
Michaux, J. R., Chevret, P., Filippucci, M. G., Macholan, M. 2002. Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: Cytochrome b and 12S rRNA. Molecular Phylogenetics and Evolution, 23, 123-136.
https://doi.org/10.1016/S1055-7903(02)00007-6
Michaux, J. R., Magnanou, E., Paradis, E., Nieberding, C., Libois, R. 2003. Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Molecular Ecology, 12, 685-697.
https://doi.org/10.1046/j.1365-294X.2003.01752.x
Michaux, J. R., Libois, R., Paradis, E., Filippucci, M. G. 2004. Phylogeographic history of the yellow-necked fieldmouse (Apodemus flavicollis) in Europe and in the Near and Middle East. Molecular Phylogenetics and Evolution, 32, 788-798.
https://doi.org/10.1016/j.ympev.2004.02.018
Michaux, J. R., Libois, R., Filippucci, M. G. 2005. So close and so different: Comparative phylogeography of two small mammal species, the Yellow‐necked fieldmouse (Apodemus flavicollis) and the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Heredity, 94, 52-63.
https://doi.org/10.1038/sj.hdy.6800561
Mohammadi, Z., Ghorbani, F., Kami, H. G., Khajeh, A., Olsson U. 2021. Molecular phylogeny of the subgenus Karstomys reveals genetic signature of post-glacial colonization of Apodemus mystacinus (Rodentia: Muridae) in the Zagros Mountains from Dierent refugia. Zoological Science, 38, 72-81.
https://doi.org/10.2108/zs200065
Musser, G. G., Carleton, M. D 2005. Superfamily Muroidea. In: Wilson, D. E., Reeder, D. A., eds. Mammal Species of the World: A geographic and taxonomic reference, 894-1531. Baltimore, MD: The John Hopkins University Press.
Orlov, V. N., Bul.va, N. Sh., Nadjafova, R. S., Kozlovsky, A. I. 1996. Evolutionary classification of European wood mice of the subgenus Sylvaemus based on allozyme and chromosome data. Bonner zoologische Beiträge, 46, 191-202.
Pages, M., Chevret, P., Gros-Balthazard, M., Hughes, S., Alcover, J. A.,Hutterer, R., Rando, J. C., Michaux, J., Hänni, C. 2012. Paleogenetic analyses reveal un suspected phylogenetic affinities between mice and the extinct Malpaisomys insularis, an endemic rodent of the Canaries. PLoS ONE. 7(2):e31123
https://doi.org/10.1371/journal.pone.0031123
Reutter, B. A., Petit, E., Brünner, H., Vogel, P. 2003. Cytochrome b haplotype divergences in West European Apodemus. Mammalian Biology, 68, 153-164.
https://doi.org/10.1078/1616-5047-00077
Suzuki, H., Filippucci, M. G., Chelomina, G. N., Sato, J. J., Serizawa, K., Nevo, E. 2008. A Biogeographic View of Apodemus in Asia and Europe Inferred From nuclear and Mitochondrial Gene Sequences. Biochemical Genetics, 46(5-6):329-46
https://doi.org/10.1007/s10528-008-9149-7
Suzuki, H., Yasuda, S. P., Sakaizumi, M., Wakana, S., Motokawa, M., Tsuchiya, K. 2004. Differential geographic patterns of mitochondrial DNA variation in two sympatric species of Japanese wood mice, Apodemus speciosus and A. argenteus. Genes & Genetic Systems, 79, 165-176.
https://doi.org/10.1266/ggs.79.165
Suzuki H., Sato J.J., Tsuchiya K., Luo J., Zhang Y.P., Wang Y.X., Jiang X.L. 2003. Molecular phylogeny of wood mice (Apodemus, Muridae) in East Asia. Biological Journal of the Linnaean Society, 80, 469-481.
https://doi.org/10.1046/j.1095-8312.2003.00253.x
Suzuki, H. Tsuchiya, К., Sakaizumi, M., Wakana, S., Gotoh, O., Saitou, N., Moriwaki, K., Sakurai, S. 1990. Differentiation of restriction sites in ribosomal DNA in the genus Apodemus II. Biochemical Genetics, 28, 137-149.
https://doi.org/10.1007/BF00561333
Tamura, K., Nei, M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512-526.
Tamura, K., Stecher, G., and Kumar, S. 2021. MEGA 11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution,
https://doi.org/10.1093/molbev/msab120
Tobe, S. S., Kitchener, A. C., Linacre, A. M. T. 2010. Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome b and cytochrome oxidase subunit I mitochondrial genes. PLoS ONE, 5 (11): e14156.
https://doi.org/10.1371/journal.pone.0014156
Vinarski, M. V. 2015. The fate of subspecies category in zoological systematics. 2. The present. Biology Bulletin Reviews, 5, 405-414 (In Russian).
https://doi.org/10.1134/S2079086415050072
Vogel, P., Maddalena, T., Mabille, A., Paquet, G. 1991. Confirmation biochimique du statut spécifique du mulot alpestre Apodemus alpicola Heinrich, 1952 (Mammalia, Rodentia). Bulletin Société Vaudoise Sciences Naturelles, 8, 471-481.
Wilson, D. E, Mittermeier, R. A, Lacher, T. E, Jr., eds. 2016. Handbook of the mammals of the world, Vol. 6. Lagomorphs and rodents 1 Barcelona. Lynx Edicions.
Yasuda, S.P., Vogel, P., Tsuchiya, K., Han, S.-H., Lin, L.-K., Suzuki, H. 2005. Phylogeographic patterning of mtDNA in the widely distributed harvest mouse (Micromys minutus) suggests dramatic cycles of range contraction and expansion during the mid- to late Pleistocene. Canadian Journal of Zoology, 83, 1411-1420.
https://doi.org/10.1139/z05-139
Young, G. R., Yap, M. W., Michaux, J. R., Steppan, S. J., Stoye, J. P. 2018. Evolutionary journey of the retroviral restriction gene Fv1. Proceeding of the National Academy of Science, 115, 10130-10135
