Advertisement

Mammalian Biology

, Volume 77, Issue 1, pp 6–12 | Cite as

Taxonomical status and phylogenetic relations between the “thomasi” and “atticus” chromosomal races of the underground vole Microtus thomasi (Rodentia, Arvicolinae)

  • M. Th. RovatsosEmail author
  • E. B. Giagia-Athanasopoulou
Original Investigation

Abstract

Laboratory crosses among wild caught individuals of the chromosomal races “atticus” and “thomasi”, were performed to analyze the degree of interracial reproductive isolation. The fertility of the studied specimens was evaluated by taking into consideration the reproductive success, the litter size and performing comparative histological examination of the testicular material. All studied populations were submitted to classical cytogenetic and mitochondrial analysis (cytochrome b gene), providing new evidences to the potential phylogenetic relations and taxonomical status of the two chromosomal races. The previously described “atticus” populations are divided in two genetically distinct, geographically and reproductively isolated lineages (2.9% total and 2.4% net divergence), which probably derived from different glacial refugia of Southern Greece. Here, we suggest that the lineage, consisting of the populations from Attiki and Evia Island, should be distinguished as a valid species, named Microtus atticus, including the two chromosomal races “atticus” and “evia”. On the contrary, the ex-“atticus” populations from North Peloponnesus belong to the same mitochondrial lineage with the other Microtus thomasi populations and should be considered as a chromosomal polymorphism inside the chromosomal race “thomasi”.

Keywords

Microtus Fertility Reproduction Cytochrome b Chromosomal race 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acosta, M.J., Marchal, J.A., Mitsainas, G.P., Rovatsos, M.T., Fernandez-Espartero, C.H., Giagia-Athanasopoulou, E.B., Sanchez, A., 2009. A new pericentromeric repeated DNA sequence in Microtus thomasi. Cytogenet. Gen. Res. 124, 27–36.CrossRefGoogle Scholar
  2. Alibert, P., Fel-Clair, F., Manolakou, K., Britton-Davidian, J., Auffray, J., 1997. Developmental stability, fitness, and trait size in laboratory hybrids between European subspecies of the house mouse. Evolution 51, 1284–1295.PubMedCrossRefPubMedCentralGoogle Scholar
  3. Barrett-Hamilton, G., 1903.Ontwo new voles of the subgenera Pitymys and Microtus. Ann. Mag. Nat. Hist. (Lond.) 7, 306–308.CrossRefGoogle Scholar
  4. Borodin, P.M., Barreiros-Gomez, S.C., Zhelezova, A.I., Bonvicino, C.R., D’Andrea, P.S., 2006. Reproductive isolation due to the genetic incompatibilities between Trichomys pachyurus and two subspecies of Trichomys apereoides (Rodentia, Echimyidae). Genome 49, 159–167.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Britton-Davidian, J., Fel-Clair, F., Lopez, J., Alibert, P., Boursot, P., 2005. Postzygotic isolation between the two European subspecies of the house mouse: Estimates from fertility patterns in wild and laboratory-bred hybrids. Biol. J. Linn. Soc. 84, 379–393.CrossRefGoogle Scholar
  6. Brunet-Lecomte, P., 1990. Liste des especes de campagnols souterrains d’Europe (Arvicolidae, Rodentia). Mammalia 54, 597–604.CrossRefGoogle Scholar
  7. Brunet-Lecomte, P., Chaline, J., 1992. Morphological convergences versus biochemical divergences in the holarctic ground voles: Terricola and Pitymys (Arvicolidae, Rodentia). N. Jb. Geol. Palaont. Mh. 12, 721–734.Google Scholar
  8. Burgos, M., Jimenez, R., Olmos, D.M., Diaz de la Guardia, R., 1988. Heterogeneous heterochromatin and size variation in the sex chromosomes of Microtus cabrerae. Cytogenet. Cell Genet. 47, 75–79.PubMedCrossRefPubMedCentralGoogle Scholar
  9. Castiglia, R., Annesi, F., Aloise, G., Amori, G., 2008. Systematics of the Microtus savii complex (Rodentia, Cricetidae) via mitochondrial DNA analyses: paraphyly and pattern of sex chromosome evolution. Mol. Phylogenet. Evol. 46, 1157–1164.PubMedCrossRefPubMedCentralGoogle Scholar
  10. Chaline, J., Graf, J.D., 1988. Phylogeny of the Arvicolidae (Rodentia): biochemical and paleontological evidence. J. Mammal. 69, 22–33.CrossRefGoogle Scholar
  11. Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L., Courant, F., 1999. Anatomy of the arvicoline radiation (Rodentia): Palaeogeographical, palaeoecological history and evolutionary data. Ann. Zool. Fenn. 36, 239–267.Google Scholar
  12. Evans, E.P., Breckon, G., Ford, C.E., 1964. An air-drying method for meiotic preparations from mammalian testes. Cytogenetics 3, 289–294.PubMedPubMedCentralGoogle Scholar
  13. Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the Boot¬strap. Evolution 39, 783–791.CrossRefGoogle Scholar
  14. Galleni, L., Tellini, A., Stanyon, R., Cicalo, A., Santini, L., 1994. Taxonomy of Microtus savii (Rodentia, Arvicolidae) in Italy: Cytogenetic and hybridization data. J. Mammal. 75, 1040–1044.CrossRefGoogle Scholar
  15. Galleni, L., Tellini, A., Cicalo, A., Fantini, C., Fabiani, O., 1998. Histological examination of the male gonad of hybrid specimens: Microtus savii x M. brachycercus (Rodentia Arvicolinae). Bonn. Zool. Beitr. 48, 1–7.Google Scholar
  16. Giagia, E.B., 1985. Karyotypes of‘44-chromosomes’ Pitymys species (Rodentia, Mammalia) and their distribution in southern Greece. Saugetierk. Mitt. 32, 169–173. Giagia-Athanasopoulou, E.B., Stamatopoulos, C., 1997. Geographical distribution and interpopulation variation in the karyotypes of Microtus (Terrricola) thomasi (Rodentia, Arvicolidae) in Greece. Caryologia 50, 303–315.Google Scholar
  17. Giagia, E.B., 1985. Karyotypes of‘44-chromosomes’ Pitymys species (Rodentia, Mammalia) and their distribution in southern Greece. Saugetierk. Mitt. 32, 169–173. Giagia-Athanasopoulou, E.B., Stamatopoulos, C., 1997. Geographical distribution and interpopulation variation in the karyotypes of Microtus (Terrricola) thomasi (Rodentia, Arvicolidae) in Greece. Caryologia 50, 303–315.CrossRefGoogle Scholar
  18. Graf, J.D., 1982. Génétique biochimique, zoogéographie et taxonomie des arvicolidae (Mammalia, Rodentia). Rev. Suisse Zool. 89, 749–787.CrossRefGoogle Scholar
  19. Golenishchev, F.N., Malikov, V.G., Nazari, F., Vaziri, A.S., Sablina, O.V., Polyakov, A.V., 2002. New species of vole of guentheri group (Rodentia, Arvicolinae, Microtus) from Iran. Russ. J. Theriol. 1, 117–123.CrossRefGoogle Scholar
  20. Hall, T.A., 1999. BioEdit: a user-friendly biological sequence alignment program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 85–98.Google Scholar
  21. Hausser, J., Fedyk, S., Fredga, K., Searle, J.B., Volobouev, V., Wojcik, J.M., Zima, J., 1994. Definition and Nomenclature of the chromosome races of Sorex araneus. Folia Zool. 43, 1–10.Google Scholar
  22. Hsu, T., Patton, J., 1969. Bone marrow preparations for chromosome studies. In: Benirschke, K. (Ed.), Comparative Mammalian Cytogenetics. Springer, pp. 454–460.Google Scholar
  23. Jaarola, M., Martínková, N., Gündüz, I., Brunhoff, C., Zima, J., Nadachowski, A., Amori, G., Bulatova, N.S., Chondropoulos, B., Fraguedakis-Tsolis, S., González-Esteban, J., José López-Fuster, M., Kandaurov, A.S., Kefelioğlu, H., Da Luz Mathias, M., Villate, I., Searle, J.B., 2004. Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol. Phylogenet. Evol. 33, 647–663.PubMedCrossRefPubMedCentralGoogle Scholar
  24. Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120.PubMedCrossRefPubMedCentralGoogle Scholar
  25. Kornilios, P., Chondropoulos, B., Fraguedakis-Tsolis, S., 2005. Allozyme variation in populations of the karyotypically polymorphic vole Microtus (Terricola) thomasi (Mammalia, Rodentia) from Greece. Belg. J. Zool 135, 175–179.Google Scholar
  26. Kratochvil, J., 1971. Der status der populationen der gattung Pitymys aus attika (Rodentia, Mammalia). Zool. Listy 20, 197–206.Google Scholar
  27. Mariolakos, I., Bantekas, I., 2002. Paleogeographical evolution of Evia Island. In: Kalemi, Kinitro E. (Ed.), Evia and Skiros: Historical documents. , pp. 16–20 (book in Greek).Google Scholar
  28. Martin, Y., Gerlach, G., Chlotterer, C., Meyer, A., 2000. Molecular phylogeny of European muroid rodents based on complete cytochrome b sequences. Mol. Phylogenet. Evol. 16, 37–47.PubMedCrossRefPubMedCentralGoogle Scholar
  29. Martinkova, N., Zima, J., Jaarola, M., Macholan, M., Spitzenberger, F., 2007. The origin and phylogenetic relationships of Microtus bavaricus based on karyotype and mitochondrial DNA sequences. Folia Zool. 56, 39–49.Google Scholar
  30. Mayr, E., 1942. Systematics and the Origin of Species from the Viewpoint of a Zoologist. Columbia University Press.Google Scholar
  31. Miller, G.S., 1910. Description of six new European mammals. Ann. Mag. Nat. Hist. (Lond.) 8, 458–461.CrossRefGoogle Scholar
  32. Mitsainas, G.P., Rovatsos, M.T., Rizou, E.I., Giagia-Athanasopoulou, E.B., 2009. Sex chromosome variability outlines the pathway to the chromosomal evolution in Microtus thomasi (Rodentia, Arvicolinae). Biol. J. Linn. Soc. 96, 685–695.CrossRefGoogle Scholar
  33. Mitsainas, G.P., Rovatsos, M.T., Giagia-Athanasopoulou, E.B., 2010. Heterochromatin study and geographical distribution of Microtus species (Rodentia, Arvicolinae) from Greece. Mamm. Biol. 75, 261–269.CrossRefGoogle Scholar
  34. Niethammer, J., 1974. Zur verbeitung und taxonomie griechscher Saügetiere. Bon. Zool. Beitr. 25, 28–55.Google Scholar
  35. Petrov, B., Zivkovic, S., 1979. Present knowledge on the systematic and distribution of Pitymys (Rodentia, Mammalia) in Yugoslavia. Biosistematica 5, 113–125.Google Scholar
  36. Posada, D., Crandall, K.A., 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
  37. Rabeder, G., 1986. Herkunft und frühe Evolution der Gattung Microtus (Arvicolidae, Rodentia). Z. Säugetierk. 51, 350–367.Google Scholar
  38. Ronquist, F., Huelsenbeck, J.P., 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.PubMedPubMedCentralCrossRefGoogle Scholar
  39. Rovatsos, M.T., Mitsainas, G.P., Stamatopoulos, C., Giagia-Athanasopoulou, E.B., 2008. First reports of XXY aneuploidy in natural populations of Thomas’pine vole Microtus thomasi (Rodentia: Arvicolidae) from Greece. Mamm. Biol. 73, 342–349.CrossRefGoogle Scholar
  40. Rovatsos, M.T., Mitsainas, G.P., Paspali, G., Oruci, S., Giagia-Athanasopoulou, E.B., 2011. Geographical distribution and chromosomal study of the underground vole Microtus thomasi in Albania and Montenegro. Mamm. Biol. 76, 22–27.CrossRefGoogle Scholar
  41. Seabright, M., 1971. A rapid banding technique for human chromosomes. Lancet 2, 971–972.PubMedPubMedCentralCrossRefGoogle Scholar
  42. Shenbrot, G.I., Krasnov, B.R., 2005. Atlas of the geographic distribution of the rarvico-line rodents of the world (Rodentia, Muridae: Arvicolinae). Pensoft Publishers.Google Scholar
  43. Spitzenberger, F., Brunet-Lecomte, P., Nadachowski, A., Bauer, K., 2000. Comparative morphometrics of the first lower molar in Microtus (Terricola) cf. liechtensteini of the Eastern Alps. Acta Theriol. 45, 471–483.CrossRefGoogle Scholar
  44. Storch, G., 2004. Late Pleistocene rodent dispersal in the Balkans. In: Griffiths, H.I., Krystufek, B., Reed, J.M. (Eds.), Balkan Biodiversity: Pattern and Process in the European Hotspot. Kluwer Academic Publishers, pp. 135–145.Google Scholar
  45. Sumner, A.T., 1972. A simple technique for demonstrating centromeric heterochromatin. Exp. Cell Res. 75, 304–306.PubMedCrossRefPubMedCentralGoogle Scholar
  46. Swofford, D.L., 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.0b10. Sinauer Associates.Google Scholar
  47. Swofford, D.L., Olsen, G.J., Waddel, P.J., Hillis, D.M., 1996. Phylogenetic inference. In: Hillis, D.M., Moritz, C., Mable, B.K. (Eds.), Molecular Systematics. Sinaue Associates, pp. 407–514.Google Scholar
  48. Tamura, K., Dudley, J., Nei, M., Kumar, S., 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596–1599.CrossRefGoogle Scholar
  49. Thelma, B.K., Juval, R.C., Tewari, R., Rao, R.S.V., 1988. Does heterochromat in variation potentiate speciation? Cytogenet. Cell Genet. 47, 204–208.CrossRefGoogle Scholar
  50. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.PubMedPubMedCentralCrossRefGoogle Scholar
  51. Tryfonopoulos, G., Thanou, E., Chondropoulos, B., Fraguedakis-Tsolis, S., 2008. mtDNA analysis reveals the ongoing speciation on Greek populations of Microtus (Terricola) thomasi (Arvicolidae, Rodentia). Biol. J. Linn. Soc. 95, 117–130.CrossRefGoogle Scholar
  52. Ventura, J., Lopez-Fuster, M.J., Cabrera-Millet, M., 1998. The cabrera vole Microtus cabrerae in Spain: a biological and morphometric approach. Neth. J. Zool. 47, 1–18.Google Scholar
  53. Walker, L.I., Spotorno, A.E., Arrau, J., 1984. Cytogenetic and reproductive studies of two nominal subspecies of Phyllotis darwini and their experimental hybrids. J. Mammal. 65, 220–230.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2011

Authors and Affiliations

  • M. Th. Rovatsos
    • 1
    Email author
  • E. B. Giagia-Athanasopoulou
    • 1
  1. 1.Section of Animal Biology, Department of BiologyUniversity of PatrasPatrasGreece

Personalised recommendations