Vol. 76 (1) 2024
ARTICLES
Genetic Variations of Growth Hormone Receptor Exon 10 in Blind Mole-Rat Superspecies (Rodentia: Spalacidae) in Turkey
Teoman Kankiliç1*, İlhan Tatyüz1, Tolga Kankiliç2, İlkay Civelek1 & Özhan Şenol1
More info
*1Department of Biotechnology, Faculty of Science and Letters, Nigde Ömer Halisdemir University, Niğde, Turkey;
E-mails: teomankankilic@gmail.com, itatyuz@gmail.com, ilkaycivelek@gmail.com, senolozhan@ohu.edu.tr
2Department of Biology, Faculty of Science, Aksaray University, Aksaray, Turkey; E-mail: tkankilic@gmail.com
Abstract
A phylogenetic analysis of 16 cytotypes in a sample of 105 blind mole-rats of the genus Nannospalax Palmer, 1903 from the entire Anatolian region has been carried out. Three superspecies (N. xanthodon, N. leucodon and N. ehrenbergi) were found to have undergone monophyletic radiations. We determined that the superspecies N. ehrenbergi and N. xanthodon contain a mixture of cryptic species distributed in the Anatolian part of Turkey. Our study indicated a fundamental split between two groups, one consisting of populations of N. ehrenbergi from the South-eastern Anatolia and the other including the remaining taxa (N. xanthodon and N. leucodon) from the remaining regions of Anatolia and from Thrace. Phylogenetic analysis indicated that there were two new unnamed cryptic species (2n=48–52 cytotype group and 2n=56 cytotype group) within the superspecies N. ehrenbergi that were reciprocally monophyletic. We reviewed species identified by traditional morphological methods to determine their taxonomic validity. We suggest that N. cilicicus (stat. n.), which is endemic to the central Anatolia, has to be considered a distinct species and not a synonym of N. xanthodon.
Key words
Nannospalax, nuclear DNA, growth hormone receptor exon 10, phylogeny
How to Cite
Kankiliç T., Tatyüz İ., Kankiliç T., Civelek İ. & Şenol Ö. 2024. Genetic Variations of Growth Hormone Receptor Exon 10 in Blind Mole-Rat Superspecies (Rodentia: Spalacidae) in Turkey. Acta zoologica bulgarica 76 (1) 11-21
References
- Adams M., Raadik T. A., Burridge C. P. & Georges A. 2014. Global biodiversity assessment and hyper-cryptic species complexes: More than one species of elephant in the room? Systematic Biology 63 (4): 518–533. https://doi.org/10.1093/sysbio/syu017
- Adkins R. M., Gelke E. L., Rowe D. & Honeycutt R. L. 2001. Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Molecular Biology and Evolution 18 (5): 777–791. doi:10.1093/oxfordjournals.molbev.a003860
- Arslan A., Kryštufek B., Matur F. & Zima J. 2016. Review of chromosome races in blind mole-rats (Spalax and Nannospalax). Folia Zoologica 65 (4): 249–301. https://doi.org/10.25225/fozo.v65.i4.a1.2016
- Bandelt H. J., Forster P. & Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16 (1): 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
- Bugarski-Stanojević V., Stamenković G., Ćirović D., Ćirić D., Stojković O., Veličković J., Kataranovski D. & Savić I. 2020. 16S rRNA gene polymorphism supports cryptic speciation within the lesser blind mole-rat Nannospalax leucodon superspecies (Rodentia: Spalacidae). Mammalian Biology 100 (3): 315–324. https://doi.org/10.1007/s42991-020-00019-9
- Chernomor O., Von Haeseler A. & Minh B. Q. 2016. Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65 (6): 997–1008. https://doi.org/10.1093/sysbio/syw037
- Coşkun Y. 1996. A new subspecies of Spalax nehringi (Satunin, 1898) (Rodentia: Spalacidae) from Turkey. Säugetierkund Mitteilungen 37: 103–109.
- Coşkun Y., Ulutürk S. & Yürümez G. 2006. Chromosomal diversity in mole-rats of the species Nannospalax ehrenbergi (Rodentia: Spalacidae) from South Anatolia, Turkey. Mammalian Biology 71 (4): 244–250. https://doi.org/10.1016/j.mambio.2006.02.005
- Csorba G., Krivek G., Sendula T., Homonnay Z. G., Hegyeli Z., Sugár S., János F., Nikola S. & Attila N. 2015. How can scientific researches change conservation priorities? A review of decade-long research on blind mole-rats (Rodentia: Spalacinae) in the Carpathian Basin. Therya 6 (1): 103–121. https://doi.org/10.12933/therya-15-245
- Doyle J. 1991. DNA protocols for plants. In: Hewitt G. M., Johnston A. W. B. & Young J. P. W. (Ed): Molecular techniques in taxonomy. Springer, Berlin, Heidelberg: pp. 283–293.
- Drummond A. J., Suchard M. A., Xie D. & Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29 (8): 1969–1973. https://doi.org/10.1093/molbev/mss075
- Excoffier L. & Lischer H. E. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10 (3): 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
- Hadid Y., Németh A., Snir S., Pavlíćek 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. http://dx.doi.org/10.1371/journal.pone.0030043
- Hall T. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 109: 95–98. https://doi.org/10.14601/Phytopathol_Mediterr-14998u1.29
- Kalyaanamoorthy S., Minh B. Q., Wong F., Von Haeseler A. & Jermiin L. S. 2017. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14 (6): 587–589. https://doi.org/10.1038/nmeth.4285
- Kandemir İ., Sözen M., Matur F., Kankılıç T., Martínková N., Çolak F., Özkurt S. Ö. & Çolak E. 2012. Phylogeny of species and cytotypes of mole-rats (Spalacidae) in Turkey inferred from mitochondrial cytochrome b gene sequences. Folia Zoologica 61 (1): 25–34. https://doi.org/10.25225/fozo.v61.i1.a5.2012
- Kankılıç T., Çolak R., Kankılıç T. & Çolak E. 2007. On the morphology and karyology of Spalax leucodon armeniacus Mehely, 1909, and Spalax leucodon cilicicus Mehely, 1909 (Mammalia: Rodentia) in Turkey. Acta Zoologica Bulgarica 59 (1): 41–46. https://doi.org/10.1111/j.1439-0264.2008.00913.x
- Kankılıç T., Çolak E. & Kankılıç T. 2009. Macro‐anatomical and karyological features of two blind mole-rat subspecies (Rodentia: Spalacidae) from Turkey. Anatomia, Histologia, Embryologia 38 (2): 145–153. https://doi.org/10.1111/j.1439-0264.2008.00913.x
- Kankılıç T., Kankılıç T., Seker P. S., Çolak R., Selvi E. & Çolak R. 2010. Contributions to the karyology and distribution areas of cytotypes of Nannospalax leucodon (Rodentia:Spalacidae) in Western Anatolia. Acta Zoologica Bulgarica 62 (2): 161–167.
- Kankılıç T., Kankılıç T., Şeker P. S. O. & Kıvanç E. 2014. Morphological and biometrical comparisons of the baculum in the genus Nannospalax Palmer, 1903 (Rodentia: Spalacidae) from Turkey with consideration of its taxonomic importance”. Turkish Journal of Zoology 38 (2): 144–157. https://doi.org/10.3906/zoo-1302-5
- Kryštufek B. & Vohralík V. 2009. Mammals of Turkey and Cyprus. Rodentia II. Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae. – Knjižnica Annales Majora: Koper, Slovenia.
- 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. Biological Journal of the Linnean Society 105 (2): 446–455. https://doi.org/10.1111/j.1095-8312.2011.01795.x
- Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35 (6): 1547. https://doi.org/10.1093/molbev/msy096
- Matur F., Yanchukov A., Çolak F. & Sözen M. 2019. Two major clades of blind mole-rats (Nannospalax sp.) revealed by mtDNA and microsatellite genotyping in Western and Central Turkey. Mammalian Biology 94 (1): 38–47. https://doi.org/ 10.1016/j.mambio.2018.11.004
- Musser G. G. & Carleton M. D. 2005. Order Rodentia. In: Wilson D. E., Reeder D. M. (Eds.) Mammal species of the world: A taxonomic and geographic reference, Johns Hopkins University Press, Baltimore, MD, USA: pp. 745–257.
- Németh A., Krnács G., Krizsik V., Révay T., Czabán D., Stojnić N., Farkas J. & Csorba G. 2013. European rodents on the edge: Status and distribution of the Vojvodina blind mole-rat. SpringerPlus 2 (1): 1–10.
- Nevo E. 2013. Stress, adaptation, and speciation in the evolution of the blind mole-rat, Spalax, in Israel. Molecular Phylogenetics and Evolution 66 (2): 515–525. https://doi.org/10.1016/j.ympev.2012.09.008
- 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”. – Proceedings of the National Academy of Sciences 91 (17): 8160–8164. https://doi.org/10.1073/pnas.91.17.816.
- Nevo E., Filippucci, M. G., Redi C., Simson S., Heth G. & Beiles A. 1995. Karyotype and genetic evolution in speciation of subterranean mole-rats of the genus Spalax in Turkey. Biological Journal of the Linnean Society 54 (3): 203–229. https://doi.org/10.1111/j.1095-8312.1995.tb01034.x
- Nevo E., Ivanitskaya E. & Beiles A. 2001. Adaptive radiation of blind subterranean mole-rats: naming and revisiting the four sibling species of the Spalax ehrenbergi Superspecies in Israel: Spalax galili (2n = 52), S. golani (2n = 54), S. carmeli (2n = 58) and S. judaei (2n = 60). Backhuys Publishers, Leiden, the Netherlands.
- Poulin R. & Pérez-Ponce de León G. 2017. Global analysis reveals that cryptic diversity is linked with habitat but not mode of life. Journal of Evolutionary Biology 30 (3): 641–649. https://doi.org/10.1111/jeb.13034
- Rozas J., Ferrer-Mata A.., Sánchez-Delbarrio J. C., Guirao-Rico S., Librado P., Ramos-Onsins S. E. & Sánchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34 (12): 3299–3302. https://doi.org/10.1093/molbev/msx248
- Savić I., Ćirović D. & Bugarski-Stanojević V. 2017. Exceptional Chromosomal Evolution and Cryptic Speciation of Blind Mole-rats Nannospalax leucodon (Spalacinae, Rodentia) from South-Eastern Europe. Genes (Basel) 8 (11): 292. https://doi.org/10.3390/genes8110292
- Savić I. R. & Nevo E. 1990. The Spalacidae: evolutionary history, speciation and population biology. Progress in Clinical and Biological Research 335:129–153.
- Sözen M. 2004. A karyological study on subterranean mole-rats of the Spalax leucodon Nordmann, 1840 superspecies in Turkey. Mammalian Biology, 69 (6): 420–429.
- Sözen M., Çolak F., Sevindik M. & Matur F. 2013. Cytotypes of Nannospalax xanthodon (Satunin, 1898) (Rodentia: Spalacidae) from western Anatolia. Turkish Journal of Zoology 37 (4): 462-469. https://doi.org/10.3906/zoo-1108-25
- Sözen M., Matur F., Çolak E., Özkurt S. & Karataş A. 2006. Some karyological records and a new chromosomal form for Spalax (Mammalia: Rodentia) in Turkey. Folia Zoologica 55 (3): 247–256.
- Steppan S., Adkins R. & Anderson J. 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology 53 (4): 533–553. https://doi.org/10.1080/10635150490468701
- Trifinopoulos J., Nguyen L. T., Von Haeseler A. & Minh B. Q. 2016. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44 (W1): 232–235. https://doi.org/10.1093/nar/gkw256
- Wilson D. E. & Reeder D. M. 2005. Mammal species of the world. A taxonomic and geographic reference. In: Wilson DE, Reeder DM (ed) A nomenclatural review, 3rd edn. Johns Hopkins University Press, Baltimore, p. 2142.
- Yang Z. & Rannala B. 1997. Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Molecular Biology and Evolution 14 (7): 717–724. https://doi.org/10.1093/oxfordjournals.molbev.a025811


