Mitochondrial Genetic Diversity and Historical Population Dynamics of the Bank Vole $Clethrionomys$ $glareolus$ in Northern Anatolia: Insights from $Cytb$ and $COI$ Gene Sequences

Yıl 2024, Cilt: 9 Sayı: 2, 483 - 501, 29.12.2024

Fatma Hümeyra Taş , Gül Olgun Karacan , Reyhan Çolak , Ercüment Çolak

https://doi.org/10.33484/sinopfbd.1522122

Öz

This study presents a genetic analysis of $Clethrionomys$ $glareolus$ populations across northern Anatolia, utilizing mitochondrial $Cytb$ and $COI$ gene sequences. Phylogenetic analysis identified two distinct Turkish clades, Clade 1 and Clade 2. Neutrality tests and mismatch distribution analyses indicate a recent population expansion following a genetic bottleneck associated with Pleistocene climatic changes. Interestingly, bank voles from Uludağ in Bursa Province of northwestern Anatolia exhibited a closer phylogenetic relationship with northeastern populations than with other northwestern populations, suggesting complex historical population dynamics, possibly involving a population replacement in northern Anatolia and relic survival in Uludağ. The geographic boundaries between the clades did not align closely with main rivers, suggesting that these geographic features did not act as strong long-term barriers to gene flow among bank vole populations. Our mtDNA study lays the foundation for future research to evaluate these scenarios using phylogeographic patterns of genome-wide diversity for a comprehensive understanding of the complex evolutionary history of bank voles in Türkiye.

Anahtar Kelimeler

Bank vole, mitochondrial DNA, Turkish Pleistocene refugia, inland water barriers, Türkiye

Etik Beyan

Ethical approval for the study was obtained from Ankara University Animal Experiments Local Ethics Committee (2019-11-108), and the research permit was acquired from the General Directorate of Nature Conservation and National Parks of the Ministry of Agriculture and Forestry (21264211-288.04-2175385).

Destekleyen Kurum

Ankara University (AUBAP-Project Number: 19L0430009).

Proje Numarası

Scientific Research Project Office of Ankara University (AUBAP-Project Number: 19L0430009)

Teşekkür

This research article incorporates information from the thesis titled "Phylogenetic Analysis of Myodes glareolus Schreber, 1780 (Mammalia: Rodentia) Distributed in Turkey," prepared by Fatma Hümeyra TAŞ. The related master's thesis was completed at the Department of Biology, Graduate School of Natural and Applied Sciences, Ankara University, on 02/26/2021

Kuzey Anadolu'da Bank Vole ($Clethrionomys$ $glareolus$) Populasyonlarının Mitokondriyal Genetik Çeşitliliği ve Tarihsel Populasyon Dinamikleri: $Cytb$ ve $COI$ Gen Dizilerinden Elde Edilen Bilgiler

Öz

Bu çalışma, Kuzey Anadolu'daki $Clethrionomys$ $glareolus$ populasyonlarının mitokondriyal $Cytb$ ve $COI$ gen dizileri kullanılarak yapılan genetik analizlerini sunmaktadır. Filogenetik analizler, iki ayrı Türkiye kladını, Klad 1 ve Klad 2'yi ayırt etmiştir. Nötralite testleri ve uyumsuzluk analizleri, Pleistosen dönemi iklim değişiklikleri ile ilişkili genetik bir darboğazın ardından yakın zamanda bir populasyon genişlemesi olduğunu ortaya koymuştur. Dikkat çekici bir şekilde, Bursa'nın Uludağ bölgesinden alınan kızıl sırtlı orman faresi örnekleri, diğer kuzeybatı populasyonları yerine kuzeydoğu populasyonları ile daha yakın filogenetik ilişkiler sergilemiştir. Bu durum, kuzey Anadolu'da potansiyel bir populasyon değişimi ve Uludağ'da bir kalıntı populasyonun hayatta kalmasını içeren karmaşık tarihsel populasyon dinamiklerine işaret etmektedir. Kladlar arasındaki coğrafi sınırlar, ana nehirlerle doğru orantılı olmayıp, bu coğrafi özelliklerin kızıl sırtlı orman faresi populasyonları arasındaki gen akışına ciddi engeller oluşturmadığını göstermektedir. Bu mitokondriyal DNA çalışması, Türkiye'deki kızıl sırtlı orman farelerinin evrimsel tarihini derinlemesine anlamak amacıyla gelecekte yapılacak araştırmalar için sağlam bir temel oluşturarak, genetik çeşitlilik gösteren filocoğrafik desenlerin kullanılmasını önermektedir.

Anahtar Kelimeler

Kızıl sırtlı orman faresi, mitokondriyal DNA, Türkiye Pleistosen sığınakları, iç su bariyerleri, Türkiye

Proje Numarası

Scientific Research Project Office of Ankara University (AUBAP-Project Number: 19L0430009)

Kaynakça

• Hewitt, G. M. (1996). Some genetic consequence of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society, 58, 247-276. https://doi.org/10.1006/bijl.1996.0035
• Hewitt, G. M. (2011). Mediterranean Peninsulas: The Evolution of Hotspots. In: Zachos, F., Habel, J. (eds) Biodiversity Hotspots. Springer, Berlin, Heidelberg.
• Kryštufek, B., Tesakov, A. S., Lebedev, V. S., Bannikova, A. A., Abramson, N. I. & Shenbrot, G. (2020). Back to the future: the proper name for red-backed voles is Clethrionomys tilesius and not Myodes Pallas. Mammalia, 84, 214-217. https://doi.org/10.1515/mammalia-2019-0067
• Deffontaine, V., Libois, R., Kotlík, P., Sommer, R., Nieberding, C., Paradis, E., Searle, B. & Michaux, J. R. (2005). Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology, 14, 1727-1739. https://doi.org/10.1111/j.1365-294X.2005.02506.x
• Deffontaine, V., Ledevin, R., Fontaine, M. C., Quere, J. P., Renaud, S., Libois, R. & Michaux, J. R. (2009). A relict bank vole lineage highlights the biogeographic history of the Pyrenean region in Europe. Molecular Ecology, 18, 2489–502. https://doi.org/10.1111/j.1365-294X.2009.04162.x
• Wójcik, J. M., Kawałko, A., Marková, S., Searle, J. B. & Kotlík, P. (2010). Phylogeographic signatures of northward post-glacial colonization from high latitude refugia: a case study of bank voles using museum specimens. Journal of Zoology, 281, 249-262. https://doi.org/10.1111/j.1469-7998.2010.00699.x
• Filipi, K., Marková, S., Searle, J. B. & Kotlík, P. (2015). Mitogenomic phylogenetics of the bank vole Clethrionomys glareolus, a model system for studying end glacial colonization of Europe. Molecular Phylogenetics and Evolution, 82, 245-57. https://doi.org/10.1016/j.ympev.2014.10.016
• Çolak, R., Karacan, G. O., Kandemir, İ., Çolak, E., Kankılıç, T., Nuri, Y. & Michaux, J. (2016). Genetic variations of Turkish bank vole, Myodes glareolus (Mammalia: Rodentia) inferred from mtDNA. Mitochondrial DNA Part A, 27, 4372-4379. https://doi.org/10.3109/19401736.2015.1089537
• Lu, T., Zhu, M., Yi, C., Si, C., Yang, C. & Chen, H. (2017). Complete mitochondrial genome of the gray redbacked vole (Myodes rufocanus) and a complete estimate of the phylogenetic relationships in Cricetidae. Mitochondrial DNA Part A, 28, 62-64. https://doi.org/10.3109/19401736.2015.1110799
• Ledevin, R., Chevret, P., Helvaci, Z., Michaux, J. R. & Renaud, S. (2018). Bank Voles in Southern Eurasia: Vicariance and Adaptation. Journal of Mammalian Evolution, 25, 119-129. https://doi.org/10.1007/s10914-016-9368-3
• Chiocchio, A., Colangelo, P., Aloise, G., Amori, G., Bertolino, S., Bisconti, R., Castiglia, R. & Canestrelli, D. (2019). Population genetic structure of the bank vole Clethrionomys glareolus within its glacial refugium in peninsular Italy. Journal of Zoological Systematical and Evolutionary Research, 57, 959-969. https://doi.org/10.1111/jzs.12289
• Kotlík, P., Deffontaine, V., Mascheretti, S., Zima, J., Michaux, J. R. & Searle, J. B. (2006). A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences, 103, 14860-14864. https://doi.org/10.1073/pnas.0603237103
• Amori, G., Contoli, L. & Nappi, A. (2008). Fauna d'Italia, Mammalia II: Erinaceomorpha, soricomorpha, lagomorpha, rodentia. Calderini, Milano.
• Osborn, D. J. (1962). Rodents of the subfamily Microtinae from Anatolia. Journal of Mammalogy, 43, 515-29. https://doi.org/10.2307/1376914
• Elmas, A. (2003). Late Cenozoic tectonics and stratigraphy of northwestern Anatolia: the effects of the North Anatolian Fault to the region. International Journal of Earth Sciences, 92, 380-396. https://doi.org/10.1007/s00531-003-0322-2
• Çolak, R., Kandemir, I., Karacan, G. O., Kankılıç, T., Çolak, E., Yiğit, N. & Özkurt, Ş. Ö. (2013). Allozyme variation in bank vole, Clethrionomys glareolus (Mammalia: Rodentia) in Northern Anatolia. Biochemical Systematics and Ecology, 50, 304-309. https://doi.org/10.1016/j.bse.2013.04.013
• Beteş, D., Çolak, R., Karacan, G. O., Kandemir, I., Kankılıç, T. & Çolak, E. (2014). Population genetic variability of Clethrionomys glareolus (Schreber, 1780) (Mammalia: Rodentia) distributed in northern Anatolia as revealed by RAPD-PCR analysis. Acta Zoologica Bulgarica, 66, 31-7.
• İbiş, O., Koepfli, K-P., Özcan, S. & Tez, C. (2023). Whole mitogenomes of Turkish white toothed shrews, genus Crocidura (Eulipotyphla: Soricidae), with new insights into the phylogenetic positions of Crocidura leucodon and the Crocidura suaveolens group. Organisms Diversity & Evolution, 23, 221-241. https://doi.org/10.1007/s13127-022-00579-3
• Tang, M. K., Jin, W., Tang, Y., Yan, C. C., Murphy, R. W., Sun, Z. Y., Zhang, X. Y., Zeng, T., Liao, R., Hou, Q. F., Yue, B. S. & Liu, S. Y. (2018). Reassessment of the taxonomic status of Craseomys and three controversial species of Myodes and Alticola (Rodentia: Arvicolinae). Zootaxa, 4429, 1-52. https://doi.org/10.11646/zootaxa.4429.1.1
• Doyle, J. J. (1990). Isolation of plant DNA from fresh tissue. Focus, 12, 13-15. https://doi.org/10.1080/09397140.2022.2058193
• 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
• Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294-299.
• Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment, editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series, 41, 95-98.
• 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 datasets. Molecular Phylogenetics and Evolution, 34, 3299-3302. https://doi.org/10.1093/molbev/msx248
• Nguyen, L-T., Schmidt, H. A., Haeseler, A. von. & Minh, B. Q. (2017). IQ-TREE: A fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution, 32, 268-274. https://doi.org/10.1093/molbev/msu300
• Huelsenbeck, J. P. & Ronquist, F. (2001). MrBayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754-755. https://doi.org/10.1093/bioinformatics/17.8.754
• Bandelt, H. J., Forster, P. & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
• Bohonak, A. J. (2002). IBD (Isolation by Distance): A program for analyses of isolation by distance. Journal of Heredity, 93, 153-154. https://doi.org/10.1093/jhered/93.2.153
• Excoffier, L. & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
• Tajima, F. (1989). The effect of change in population size on DNA polymorphism. Genetics, 123, 597-601. https://doi.org/10.1093/genetics/123.3.597
• Fu, Y. X. (1997). Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 147, 915-25. https://doi.org/10.1093/genetics/147.2.915
• Honda, A., Murakami, S., Harada, M., Tsuchiya, K, Kinoshita, G. & Suzuki, H. (2019). Late Pleistocene climate change and population dynamics of Japanese Myodes voles inferred from mitochondrial cytochrome b sequences. Journal of Mammalogy, 100, 1156-1168. https://doi.org/10.1093/jmammal/gyz093
• Suzuki, Y., Tomozawa, M., Koizumi, Y., Tsuchiya, K. & Suzuki, H. (2015). Estimating the molecular evolutionary rates of mitochondrial genes referring to quaternary ice age events with inferred population expansions and dispersals in Japanese Apodemus. BMC Evolutionary Biology, 15, 187. https://doi.org/10.1186/s12862-015-0463-5
• Hanazaki, K., Tomozawa, M., Suzuki, Y., Kinoshita, G., Yamamoto, M., Irino, T. & Suzuki, H. (2017). Estimation of evolutionary rates of mitochondrial DNA in two Japanese wood mouse species based on calibrations with quaternary environmental changes. Zoological Science, 34, 201-210. https://doi.org/10.2108/zs160169
• Ho, S. Y. W., Phillips, M. J., Cooper, A. & Drummond, A. J. (2005). Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Molecular Biology and Evolution, 22, 1561-1568. https://doi.org/10.1093/molbev/msi145
• Kotlík, P., Deffontaine, V., Mascheretti, S., Zima, J., Michaux, J. R. & Searle, J. B. (2006). A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences, 103, 14860-14864. https://doi.org/10.1073/pnas.0603237103
• Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, Massachussets.
• Searle, J. B., Kotlík, P., Rambau, R. V., Marková, S., Herman, J. S., and McDevitt, A. D. (2009). The Celtic fringe of Britain: insights from small mammal phylogeography. Proceedings of the Royal Society B: Biological Sciences, 276, 4287-4294. https://doi.org/10.1098/rspb
• Kotlík, P., Marková, S., Konczal, M., Babik, W., Searle, J. B. (2018). Genomics of end-Pleistocene population replacement in a small mammal. Proceedings of the Royal Society B: Biological Science, 285, 20172624. https://doi.org/10.1098/rspb.2017.2624
• Marková, S., Horníková, M., Lanier, H. C., Henttonen, H., Searle, J. B., Weider, L. J. & Kotlík, P. (2020). High genomic diversity in the bank vole at the northern apex of a range expansion: The role of multiple colonizations and end-glacial refugia. Molecular Ecology, 29, 1730-1744. https://doi.org/10.1111/mec.15427
• Kotlík, P., Marková, S., Vojtek, L., Stratil, A., Šlechta, V., Hyršl, P. & Searle, J. B. (2014). Adaptive phylogeography: functional divergence between haemoglobins derived from different glacial refugia in the bank vole. Proceedings of the Royal Society B: Biological Science, 281, 20140021. https://doi.org/10.1098/rspb.2014.0021
• Ledevin, R., Chevret, P., Helvaci, Z., Michaux, J.R. & Renaud, S. (2018). Bank Voles in Southern Eurasia: Vicariance and Adaptation. Journal of Mammalian Evolution, 25, 119-129. https://doi.org/10.1007/s10914-016-9368-3
• İbiş, O., Selçuk, A. Y., Teber, S., Baran, M., Kaya, A., Özcan, S., Kefelioğlu, H. & Tez, C. (2022). Complete mitogenomes of Turkish tree squirrels, Sciurus anomalus and S. vulgaris, (Sciuridae: Rodentia: Mammalia) and their phylogenetic status within the tribe Sciurini, Gene, 841. https://doi.org/10.1016/j.gene.2022.146773
• Demirtaş, S. (2022). Phylogeographic structure of the Persian Squirrel, Sciurus anomalus Güldenstädt, 1785 (Mammalia: Rodentia) in the Anatolian Peninsula, based on mitochondrial DNA sequences: implications for metapopulation. Zoology in the Middle East, 68, 95-108. https://doi.org/10.1080/09397140.2022.2058193
• Kankılıç, T., Şeker, P. S., Erdik, A. C., Kankılıç, T., Selvi, E., Yiğit, N. & Çolak, E. (2018). Determination of genetic variations in the genus Dryomys Thomas, 1906 (Rodentia: Gliridae) distributed in Anatolia using NADH dehydrogenase 1 (ND1) gene. Mitochondrial DNA Part A, 29, 933-942. https://doi.org/10.1080/24701394.2017.1389915
• Neumann, K., Yiğit, N., Fritzsche, P., Çolak, E., Feoktistova, N., Surov, A. & Michaux, J. (2017). Genetic structure of the Turkish hamster (Mesocricetus brandti). Mammalian Biology, 86, 84-91. https://doi.org/10.1016/j.mambio.2017.06.004
• Baker, R. J. & Bradley, R. D. (2006). Speciation in Mammals and the Genetic Species Concept. Journal of Mammalogy, 87, 643-662. https://doi.org/10.1644/06-MAMM-F-038R2.1
• Ramírez-Soriano, A., Ramos-Onsins, S. E., Rozas, J., Calafell, F. & Navarro, A. (2008). Statistical power analysis of neutrality tests under demographic expansions, contractions and bottlenecks with recombination. Genetics, 179, 555-67. https://doi.org/10.1534/genetics.107.083006
• Riemsdijk, I. V., Arntzen, J. W., Bogaerts, S., Franzen, M., Litvinchuk, S. N., Olgun, K. & Wielstra, B. (2018). The Near East as a cradle of biodiversity: A phylogeography of banded newts (Genus Ommatotriton) reveals extensive inter and intraspecific genetic differentiation. Molecular Phylogenetics and Evolution, 114, 73-81. https://doi.org/10.1016/j.ympev.2017.05.028
• Wielstra, B., Espregueira Themudo, G., Güclü, Ö., Olgun, K., Poyarkov, N. A. & Arntzen, A. Z. (2010). Cryptic crested newt diversity at the Eurasian transition: the mitochondrial DNA phylogeography of Near Eastern Triturus newts. Molecular Phylogenetics and Evolution, 56, 888-896. https://doi.org/10.1016/j.ympev.2010.04.030
• Wielstra, B., Baird, A. B. & Arntzen, J. W. (2013). A multimarker phylogeography of crested newts (Triturus cristatus superspecies) reveals cryptic species. Molecular Phylogenetics and Evolution, 67, 167-175. https://doi.org/10.1016/j.ympev.2013.01.009
• Wielstra, B., Burke, T., Butlin, R. K., Avcı, A., Üzüm, N., Bozkurt, E., Olgun, K. & Arntzen, J. W. (2017). A genomic footprint of hybrid zone movement in crested newts. Evolution Letters, 1(2), 93-101. https://doi.org/10.1002/evl3.9
• Helvacı, Z., Renaud, S., Ledevin, R., Adriaens, D., Michaux, J., Çolak, R., Kankılıç, T., Kandemir, İ., Yiğit, N. & Çolak, E. (2012). Morphometric and genetic structure of the edible dormouse (Glis glis): a consequence of forest fragmentation in Anatolia. Biological Journal of the Linnean Society, 107, 611-623. https://doi.org/10.1111/j.1095-8312.2012.01952.x
• Kaya, S. & Çıplak, B. (2017). Phylogeography and taxonomy of the Psorodonotus caucasicus (Orthoptera, Tettigoniidae) group: independent double invasion of the Balkans from the Caucasus. Systematic Entomology, 42, 118-133. https://doi.org/10.1111/syen.12197
• Karacan, G. O., Çolak, R. & Çolak, E. (2021). The roles of possible geographic barriers and geological events on the phylogeographic structure of the Eastern broad toothed field Mouse (Apodemus mystacinus). Mammalia, 85, 401-411. https://doi.org/10.1515/mammalia-2020-0017