Mammalian Biology

, Volume 94, Issue 1, pp 38–47 | Cite as

Two major clades of blind mole rats (Nannospalax sp.) revealed by mtDNA and microsatellite genotyping in Western and Central Turkey

  • Ferhat MaturEmail author
  • Alexey Yanchukov
  • Faruk Çolak
  • Mustafa Sözen
Original investigation


The Anatolian and the Lesser blind mole rats (Nannospalax xanthodon and N. leucodon) are widely distributed in Anatolia and Thrace and feature remarkable diversity of chromosomal races. The evolutionary relationship among various cytotypes has not been fully resolved, and little is known about the genetic diversity at the population level. Traditionally, N. xanthodon is divided into Western and Central Anatolian phylogenetic clades, but the inclusion of particular cytotypes into one or the other clade still causes controversy, and the relationship of N. leucodon from Thrace to other Turkish populations is not known. We genotyped 67 and 62 individuals, sampled across Western Turkey, respectively at one mtDNA (1048 bp long fragment of cyt b) and ten highly polymorphic microsatellite markers. The population genetic structure was analyzed (i) in respect to previously assigned karyotype (cytotypes 2n = 38, 50, 52, 56 and 60 of N. xanthodon and 2n = 56 of N. leucodon) and geographic locality data, and (ii) without assuming any prior grouping. Both the phylogeny constructed from the cyt b sequence and the population structure revealed by the microsatellite genotyping revealed the presence of two major clades. The first included the Western Anatolian populations of N. xanthodon (cytotypes 2n = 38, 2n = 50 and 2n = 52), but also N. leucodon from Thrace (2n = 56). The second clade included the Central Anatolian populations of N. xanthodon with cytotypes 2n = 56 and 2n=60. These findings support and refine the previously suggested relationships between 2n = 38, Thracian N. leucodon and 2n = 60 (Hadid et al., 2012). We also revealed higher genetic diversity, particularly within cytotype 2n = 38 (race anatolicus), and stronger population structuring within the Western Anatolian clade. In contrast, the microsatellite genotypes of two races in Central Anatolian clade (2n = 60 and 2n = 56 from Manisa province), showed less diversity and weaker population structure.


Rodents Microsatellites Population structure Cytochrome b Phylogeny 


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  1. Archer, F.I., Adams, P.E., Schneiders, B.B., 2017. Stratag: An R Package for Manipulating, summarizing and analysing population genetic data. Mol.Ecol. Res. 17 (2), 5–11, Scholar
  2. Arslan, A., Kryštufek, B., Matur, F., Zima, J., 2016. Review of chromosome races in blind mole rats (Spalax and Nannospalax). Folia Zool. 65, 249–301, Scholar
  3. Bryja, J., Konvičková, H., Bryjová, A., Mikula, O., Makundi, R., Chitaukali, W.N., Sumbera, R., 2018. Differentiation underground: Range-wide multilocus genetic structure of the silvery mole-rat does not support current taxonomy based on mitochondrial sequences. Mamm. Biol. 93, 82–92, Scholar
  4. Darriba, D., Taboada, G.L., Doallo, R., Posada, D., 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9, 772,
  5. Dobigny, G., Britton-Davidian, J., Robinson, T.J., 2017. Chromosomal polymorphism in mammals: an evolutionary perspective. Biol. Rev. 92, 1–21, Scholar
  6. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software structure: a simulation study. Mol. Ecol. 14, 2611–2620, Scholar
  7. Falush, D., Stephens, M., Pritchard, J.K., 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 64, 1567-LP-1587.Google Scholar
  8. Felsenstein, J., 1985. Phytogenies and the comparative method. Am. Nat. 125, 1–15, Scholar
  9. Goudet, J., 2005. hierfstat, a package for R to compute and test hierarchical F-statistics. Mol. Ecol. Notes 5, 184–186, Scholar
  10. Guichoux, E., Lagache, L., Wagner, S., Chaumeil, P.P.L., Lepais, O., Lepoittevin, C., Malausa, T., Revardel, E.F.S., Petit, R.J., 2011. Current trends in microsatellite genotyping. Mol. Ecol. Resour. 11, 591–611, Scholar
  11. Guindon, S., Gascuel, O., 2003. A Simple, Fast and Accurate Method to estimate large phytogenies by maximum-likelihood. Syst. Biol. 52, 696–704.CrossRefGoogle Scholar
  12. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., Gascuel, O., 2010. New algorithms and methods to estimate maximum-likelihood phytogenies: Assessing the Performance of PhyML 3.0. Syst. Biol. 59, 307–321, Scholar
  13. Hadid, Y., Németh, A., Snir, S., Pavlíček, T., Csorba, G., Kázmér, M., Major, Á., Mezhzherin, S., Rusin, M., Coşkun, Y., Nevo, E., 2012. Is evolution of blind mole rats determined by climate oscillations? PLoS One 7, e30043,
  14. Hedrick, P.W., 2005. A standardized genetic differentiation measure. Evolution (N.Y) 59, 1633–1638, Scholar
  15. Ivanitskaya, E., Sozen, M., Rashkovetsky, L., Matur, F., Nevo, E., 2008. Discrimination of 2n = 60 Spalax leucodon cytotypes (Spalacidae, Rodentia) in Turkey by means of classical and molecular cytogenetic techniques. Cytogenet. Genome Res. 122, 139–149, Scholar
  16. Jakobsson, M., Rosenberg, N.A., 2007. CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23, 1801–1806, Scholar
  17. Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405, Scholar
  18. Kandemİr, İ., Sözen, M., Matur, F., Kankoiloiç, T., Martínková, N., Çolak, F., Özkurt Ö, S., Çolak, E., 2012. Phytogeny of species and cytotypes of mole rats (Spalacidae) in Turkey inferred from mitochondrial cytochrome b gene sequences. Folia Zool 61, 25–33, Scholar
  19. Kankoiloiç, T., Kankoiloiç, T., Çolak, R., Çolak, E., Karataş, A., 2007. Karyological comparison of populations of the Spalax leucodon Nordmann, superspecies (Rodentia: Spalacidae) in Turkeyl. Zool. Middle East 42, 15–24, Scholar
  20. Kankoiloiç, T., Kankoiloiç, T., Sözen, M., Çolak, E., 2015. Allozyme variations in Anatolian populations and cytotypes of the blind mole rats (Nannospalax). Biochem. Syst. Ecol. 59, 126–134, Scholar
  21. Karanth, K.P., Avivi, A., Beharav, A., Nevo, E., 2004. Microsatellite diversity in populations of blind subterranean mole rats (Spalax ehrenbergi superspecies) in Israel: speciation and adaptation. Biol. J. Linn. Soc. 83, 229–241, Scholar
  22. Kraemer, P., Gerlach, G., 2017. Demerelate: calculating interindividual relatedness for kinship analysis based on codominant diploid genetic markers using R. Mol. Ecol. Resour. 17, 1371–1377, Scholar
  23. Kryštufek, B., Vohralík, V., 2009. Mammals of Turkey and Cyprus. Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyida, Hystricidae, Castoridae. Annales Majora. Annales Majora, Koper.Google Scholar
  24. Kryštufek, B., Ivanitskaya, E., Arslan, A., Arslan, E., Bužan, E.V., 2012. Evolutionary history of mole rats (Genus Nannospalax) inferred from mitochondrial cytochrome b sequence. Biol. J. Linn. Soc. 105, 446–455, Scholar
  25. Leberg, P.L., 2008. Estimating allelic richness: Effects of sample size and bottlenecks. Mol. Ecol. 11, 2445–2449, Scholar
  26. Lecompte, E., Brouat, C., Duplantier, J.M., Galan, M., Granjon, L., Loiseau, A., Mouline, K., Cosson, J.F., 2005. Molecular identification of four cryptic species of Mastomys (Rodentia, Murinae). Biochem. Syst. Ecol. 33, 681–689, Scholar
  27. Legendre, P., Fortin, M.J., 1989. Spatial pattern and ecological analysis. Vegetatio 80, 107–138, Scholar
  28. Matur, F., Çolak, F., Ceylan, T., Sevindik, M., Sözen, M., 2013. Chromosomal evolution of the genus Nannospalax (Palmer (Rodentia, Muridae) from western Turkey. Turkish J. Zool., 37,
  29. Meirmans, P.G., 2006. Using the amova framework to estimate a standardized genetic differentiation measure, Evolution. Evolution (N.Y) 60, 2399–2402, Scholar
  30. Michaux, J., 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. Mol. Phylogenet. Evol. 23, 123–136, Scholar
  31. El Mousadik, A., Petit, R.J., 1996. High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor. Appl. Genet. 92, 832–839, Scholar
  32. Nevo, E., Filippucci, M.G., Redi, C., Korol, A., Beiles, A., 1994. Chromosomal speciation and adaptive radiation of mole-rats in Asia minor correlated with increased ecological stress. Proc. Natl. Acad. Sci. U. S. A. 91, 8160–8164.CrossRefGoogle Scholar
  33. Page, R.D.M., 1996. TreeView: An Application to Display Phylogenetic Trees on Personal Computers. Comput. Ap (12), 357–358, SRC-Baidu Scholar FG-0.Google Scholar
  34. Rambaut, A., Drummond, A.J., Xie, D., Baele, G., Suchard, M.A., 2018. Posterior summarization in Bayesian phylogenetics using tracer 1. 7. Syst. Biol. 67, 901–904, Scholar
  35. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P., 2012. MrBayes 3. 2: Efficient bayesian phylogenetic önference and model choice across a large model space. Syst. Biol. 61, 539–542, Scholar
  36. Rosas, U., Barton, N.H., Copsey, L., Barbier de Reuille, P., Coen, E., 2010. Cryptic variation between species and the basis of hybrid performance. PLoS Biol. 8, el000429, Scholar
  37. Sözen, M., Çolak, F., Sevindik, M., Matur, F., 2015. Two new cytotypes and additional karyological records for blind mole rats, Nannospalax xanthodon and n. ehrenbergi (Mammalia, Rodentia) in Turkey. Folia Zool, 64.Google Scholar
  38. Sozen, M., Matur, F., Colak, E., Ozkurt, S., Karatas, A., 2006. Some karyological records and a new chromosomal form for Spalax (Mammalia: Rodentia) in Turkey. Folia Zool 55, 247–256.Google Scholar
  39. Stamatakis, A., 2014. RAxML Version 8: A Tool for Phylogenetic analysis and post-analysis of large phytogenies. Bioinformatics 30 (9). Oxford University Press, pp. 1312–1313, Scholar
  40. Šumbera, R., Krásová, J., Lavrenchenko, L.A., Mengistu, S., Bekele, A., Mikula, O., Bryja, J., 2018. Ethiopian highlands as a cradle of the African fossorial root-rats (genus Tachyoryctes), the genetic evidence. Mol. Phylogenet. Evol. 126, 105–115, Scholar
  41. Swofford, D.L., 2002. PAUP* Phylogenetic Analysis using parsimony (* and other methods). Version 4. Sinauer Associates, Massachusetts.Google Scholar
  42. Tamura, I., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 30, 2725–2729, Scholar
  43. Wahrman, J., Goitein, R., Nevo, E., 1969. Mole rat Spalax: Evolutionary significance of chromosome variation. Science 164, 82–84, Scholar
  44. Warren, D.L., Geneva, A.J., Lanfear, R., Rosenberg, M., 2017. RWTY (R We There Yet): An R Package for Examining convergence of bayesian phylogenetic analyses. Mol. Biol. Evol. 34, 1016–1020, Scholar
  45. Winter, D.J., 2012. mmod: an R library for the calculation of population differentiation statistics. Mol. Ecol. Resour. 12, 1158–1160, Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2019

Authors and Affiliations

  • Ferhat Matur
    • 1
    • 2
    Email author
  • Alexey Yanchukov
    • 3
  • Faruk Çolak
    • 3
  • Mustafa Sözen
    • 3
  1. 1.Faculty of Science, Department of Biology, BucaDokuz Eyül UniversityIzmirTurkey
  2. 2.The Center for Faunistic and Floristic Research, BucaDokuz Eyül UniversityIzmirTurkey
  3. 3.Faculty of Arts and Science, Department of BiologyBülent Ecevit UniversityZonguldakTurkey

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