Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)

Microtus daghestanicus (Shidlovskiy, 1919), one of the least studied members of the subgenus Terricola “subterraneus" species group, remains poorly understood with respect to its phylogeography and genetic structure. Here, we reevaluated its evolutionary relationships, genetic diversity and...

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Дата:	2026
Автори:	Kalkan , K. K., Çetintaş , O., Çolak , F., Yanchukov , A., Sözen , M.
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author	Kalkan , K. K. Çetintaş , O. Çolak , F. Yanchukov , A. Sözen , M.
author_facet	Kalkan , K. K. Çetintaş , O. Çolak , F. Yanchukov , A. Sözen , M.
author_institution_txt_mv	[ { "author": "K. K. Kalkan ", "institution": "Department of Biology, Faculty of Sciences, Türkiye " }, { "author": "O. Çetintaş ", "institution": "Wildlife Research Institute, Ondokuz Mayıs University, Türkiye" }, { "author": "F. Çolak ", "institution": "Department of Biology, Faculty of Sciences, Türkiye " }, { "author": "A. Yanchukov ", "institution": "Department of Biology, Faculty of Sciences, Türkiye " }, { "author": "M. Sözen ", "institution": "Department of Biology, Faculty of Sciences, Türkiye " } ]
author_sort	Kalkan , K. K.
baseUrl_str	https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/oai
collection	OJS
datestamp_date	2026-06-29T16:20:36Z
description	Microtus daghestanicus (Shidlovskiy, 1919), one of the least studied members of the subgenus Terricola “subterraneus" species group, remains poorly understood with respect to its phylogeography and genetic structure. Here, we reevaluated its evolutionary relationships, genetic diversity and distribution of the species using mitochondrial cytb sequences (71 haplotypes of 77 samples) together with new field records from Türkiye. Maximum-likelihood and Bayesian analyses produced nearly similar topologies and separated three well-defined lineages corresponding to M. daghestanicus, M. fingeri (Neuhäuser, 1936), and M. subterraneus (Sélys, 1836). Two mitochondrial lineages were identified within M. daghestanicus: a Caucasian lineage (Russia–Georgia) and an Anatolian lineage including Ardahan, Artvin, Kars, and a newly recorded population from Hakkari. The Hakkari record represents the first verified occurrence of the species in southern part of Eastern Anatolia and marks the southern limit of the species’ known range, extending the known distribution and highlighting the Anatolia–Caucasus phylogeographic separation. Pairwise K2P distances and Fst values indicated pronounced genetic differentiation among taxa, whereas neutrality tests showed no significant deviations from mutation–drift equilibrium. Generally, observed genetic structure is consistent with long-term geographic isolation across the Pontic–Caucasian region. Our results provide a foundation for understanding the taxonomy and distribution of M. daghestanicus.
doi_str_mv	10.15407/zoo2026.03.245
first_indexed	2026-06-30T01:00:32Z
format	Article
fulltext	DOI 10.15407/zoo2026.03.245 UDC 599.323.45:575.86:591.9(479+560-11) PHYLOGEOGRAPHY OF TERRICOLA VOLES IN THE CAUCASUS AND EASTERN ANATOLIA, WITH A NEW SOUTHERNMOST RECORD OF MICROTUS DAGHESTANICUS (RODENTIA, CRICETIDAE, ARVICOLINAE) K. K. Kalkan 1,, O. Çetintaş 2, F. Çolak 1, A. Yanchukov 1 & M. Sözen 1 1 Department of Biology, Faculty of Sciences, Zonguldak Bülent Ecevit University, Zonguldak 67100, Türkiye 2 Wildlife Research Institute, Ondokuz Mayıs University, Samsun 55270, Türkiye Corresponding author E-mail: kursatkenankalkan@gmail.com K. K. Kalkan (https://orcid.org/0000-0003-3065-2256) O. Çetintaş (http://orcid.org/0000-0001-7601-2540) F. Çolak (http://orcid.org/0000-0003-3985-7864) A. Yanchukov (http://orcid.org/0000-0002-9613-8770) M. Sözen (http://orcid.org/0000-0002-1911-605X) urn:lsid:zoobank.org:pub:141EA947-72B4-453B-9245-9CED2E02F3B7 Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New South- ernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae). Kalkan, K. K., Çetintaş, O., Çolak, F., Yanchukov, A., Sözen, M. — Microtus daghestanicus (Shidlovskiy, 1919), one of the least studied members of the subgenus Terricola ‘subterraneus’ species group, remains poorly understood with respect to its phylogeography and genetic structure. Here, we reevaluated its evolutionary relationships, genetic diversity and distribution of the species using mitochon- drial cytb sequences (71 haplotypes of 77 samples) together with new field records from Türkiye. Maximum-likelihood and Bayesian analyses produced nearly similar topologies and separated three well-defined lineages corresponding to M. daghestanicus, M. fingeri (Neuhäuser, 1936), and M. subterraneus (Sélys, 1836). Two mitochondrial lineages were identified within M. daghestani- cus: a Caucasian lineage (Russia–Georgia) and an Anatolian lineage including Ardahan, Artvin, Kars, and a newly recorded population from Hakkari. The Hakkari record represents the first verified occurrence of the species in southern part of Eastern Anatolia and marks the south- ern limit of the species’ known range, extending the known distribution and highlighting the Anatolia–Caucasus phylogeographic separation. Pairwise K2P distances and Fst values indicated Fauna and Systematics Zoodiversity, 60(3): 245–266, 2026 © Publisher Publishing House “Akademperiodyka” of the NAS of Ukraine, 2026. The article is published under an open access license CC BY-NC-ND (https://creativecommons.org/licenses/ by-nc-nd/4.0/) ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 246 pronounced genetic differentiation among taxa, whereas neutrality tests showed no significant deviations from mutation–drift equilibrium. Generally, observed genetic structure is consistent with long-term geographic isolation across the Pontic–Caucasian region. Our results provide a foundation for understanding the taxonomy and distribution of M. daghestanicus. Key words: Arvicolinae, cytochrome b, phylogeny, small mammals. Introduction The subfamily Arvicolinae is among the most species-rich and rapidly evolving lin- eages within the muroid rodents (McKenna & Bell, 1997; Chaline et al., 1999; Muss- er & Carleton, 2005). Within this subfamily, Microtus is the most speciose genus and taxonomically one of the most complex groups (Jaarola et al., 2004; Baskevich et al., 2016, 2017; Bogdanov et al., 2021, 2024). It is represented by five subgenera and 37 species in the Palearctic and 60 species across the Holarctic region (Kryštufek & Shenbrot, 2022; MDD, 2025). In Türkiye, Microtus is known to include 11 species (Kryštufek & Shenbrot, 2022; Sözen & Çolak, 2025). Several subgenera and species groups within Microtus have speciated across different parts of its wide distribution range, and there are still many groups in the process of speciation (Jaarola et al., 2004). Pine voles are now recognized as members of the subgenus Terricola, a Palearctic taxon distributed across the Caucasus and much of Europe, living in both lowland and mountainous habitats (e. g., Chaline, 1987; Jaarola et al., 2004; Baskevich et al., 2016; Kryštufek & Shenbrot, 2022). According to Kryštufek & Shenbrot (2022), there are 14 recognized species within the subgenus Terricola, although their taxo- nomic status remains a subject of debate. The ‘subterraneus’ species group includes M. subterraneus (Sélys, 1836), found across Asia Minor and Europe, M. fingeri (Neuhäuser, 1936) in northern Anatolia, and M. daghestanicus (Shidlovskiy, 1919) in the Caucasus mountains (Jaarola et al., 2004; Baskevich et al., 2016, 2017; Bogdanov et al., 2021, 2024; Çetintürk, 2022; Kryštufek & Shenbrot, 2022). Cytogenetic studies have revealed substantial chromo- somal variation within the group, with M. daghestanicus displaying particularly high polymorphism (2n = 38–54) compared to the stable karyotypes of M. subterraneus and M. fingeri (e. g., Ivanov & Tembotov, 1972; Akhverdyan et al., 1992; Macholán et al., 2001; Baskevich et al., 2007, 2018; Selçuk & Kefelioğlu, 2024). Subsequent molecular studies have shown that M. subterraneus, M. fingeri, and M. daghestanicus are genetically distinct (e. g., Macholán et al., 2001; Jaarola et al., 2004; Tougard, 2017; Bogdanov et al., 2021). While earlier studies debated the posi- tion of M. majori, recent multilocus and karyological assessments have confirmed that it constitutes a separate species group, leaving M. subterraneus, M. daghestani- cus, and the recently recognized northern Anatolian endemic M. fingeri as the sole members of the ‘subterraneus’ species group (e. g., Baskevich, 1997; Mezhzherin et al., 1995; Jaarola et al., 2004; Tougard, 2017; Bogdanov et al., 2021). Thus, the ‘subter- raneus’ species group of the subgenus Terricola currently includes three species: M. subterraneus (European Pine Vole); M. fingeri (Anatolian Pine Vole); and M. daghetanicus (Dagestan Pine Vole) (Kryštufek & Shenbrot, 2022; MDD, 2025). In contrast to the extensively sampled Caucasian populations, data from Türkiye remain scarce and limited to a few localities in the northeast (Jaarola et al., 2004; Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 247 Çetintürk, 2022). Caucasian populations of the species have been sampled much better (e. g., Ivanov & Tembotov, 1972; Akhverdyan et al., 1992; Bulatova et al., 2007; Baskevich et al., 2017; Bogdanov et al., 2024) but to date, no detailed phylogeograph- ic study has addressed the species’ distribution limits in Anatolia or its genetic con- nectivity with the main Caucasian range. Such limited representation of Anatolian populations and insufficient distribution data in the existing literature highlight the importance of the present study. Here, we focus on the Caucasus–Eastern Anatolia region and integrate newly collected Turkish cytb sequences with publicly available data to update the phyloge- ographic framework for M. daghestanicus. Our goal was (1) to identify new distribu- tion areas for M. daghestanicus in Türkiye, (2) to assess the genetic diversity and phylogenetic relationships of newly identified Anatolian populations in respect to the existing data, and (3) to gain better insight into the phylogeographic structure of M. daghestanicus across its range. Material and Methods Samples A total of 77 samples belonging to the subgenus Terricola were examined in this study (22 from M. subterraneus, 9 from M. fingeri, and 46 from M. daghestanicus). Additionally, two M. arvalis (Pallas, 1778) samples were included as the outgroup. Eleven out of 46 M. daghestanicus samples were collected by us from the Eastern Black Sea (Artvin) and Eastern Anatolia (Ardahan and Hakkari) regions (Fig. 1 and Table 1). Additional sequences (M. subterraneus, M. fingeri, M. daghestanicus, and M. arvalis) were obtained from GenBank. The distribution (areal) layer was redrawn based on the distribution information in Kryštufek & Shenbrot (2022) and com- bined with our sampling localities for visualization purposes. Sampling of M. daghestanicus was conducted under permits issued by the Min- istry of Agriculture and Forestry, Republic of Türkiye, General Directorate of Nature Conservation and National Parks (Permit Numbers: E-21264211-288.04-10350129 and E-72784983-288.04-19227738). Animal ethics approval was granted by the Eth- ics Committee of Zonguldak Bülent Ecevit University (Zonguldak, Türkiye) (Permit Numbers: 91330202-09 and 2025-03-20/02). Fieldwork was carried out during the summer periods, and the samples were cap- tured at elevations ranging from 2178 m to 3324 m. Tissues including lung, liver, heart, spleen, and kidney were preserved in RNAlater solution and stored at –80 °C until molecular analysis. Skulls were cleaned and are currently being kept with registration numbers in our mammal collection at Zonguldak Bülent Ecevit University. Molecular DNA Analys is DNA was extracted from the liver tissue samples preserved in RNALater, using EcoPURE Genomic DNA Kit (EcoTech, Erzurum, Türkiye) following the manufac- turer’s protocol. The mitochondrial cytb gene was amplified by using the primer pair L7 (5'-ACCAATGACATGAAAAATCATCGTT-3') and H6 (5'-TCTCCATTTCTG- GTTTACAAGAC-3') (Montgelard et al., 2002). K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 248 Fig. 1. Map showing the sample localities of subgenus Terricola (‘subterraneus’ species group) included in the present study: M. subterraneus; M. fingeri; M. daghestanicus (Anatolia); M. daghestanicus (Western Greater Caucasus); M. daghestanicus (Central and Eastern Greater Caucasus); M. daghestanicus (Anatolia, this study). Locality numbers correspond to Table 1. Only the symbol represents samples newly sequenced in this study; all other localities represent sequences obtained from GenBank. The shaded area colors follow the branch colors in Fig. 2. The distribution (areal) layer was redrawn based on the distribution information in Kryštufek & Shenbrot (2022) and combined with our sampling localities for visualization purposes Each PCR reaction was prepared in a final volume of 25 µl, containing 2.5 µl 10× Taq buffer, 0.5 µl dNTP mixture, 0.25 µl Taq DNA polymerase, 1.5 µl MgCl₂, 0.5 µl DNA template, 0.5 µl of each primer, and 18.75 µl nuclease-free water. Amplifications were conducted in a gradient thermal cycler under the following conditions: an initial dena- turation at 95 °C for 5 min; 35 cycles of denaturation at 95 °C for 30 s, annealing at 55 °C for 60 s, and extension at 72 °C for 90 s; followed by a final extension at 72 °C for 10 min. PCR products were purified using the EcoPURE PCR/Gel Purification Kit (Eco- Tech, Erzurum, Türkiye) according to the manufacturer’s instructions. All DNA ex- traction and PCR purification steps were carried out under sterile conditions to pre- vent contamination. The purified products were sequenced in both directions by Macrogen Europe (Amsterdam, The Netherlands). Phylogenet ic Analys is All sequences were edited and assembled using Geneious Prime software v.2025.2.1 (Ge- neious Biomatters Ltd., 2025; https://www.geneious.com), and multiple sequence align- ment was performed with the MAFFT v.7 (Katoh & Standley, 2013) algorithm imple- mented in the same software. To explore the phylogenetic relationships, we used 77 cytb sequences representing M. subterraneus, M. fingeri, and M. daghestanicus, together with two M. arvalis (GenBank: AM991045 [Tougard, 2008b] and AY220788 [Haynes et al., Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 249 Table 1 . Sampling localities (also shown on Fig. 1) with the corresponding cytb haplotypes Map Number Collection Number Haplotype Number GenBank Accession Number Locality References M. daghestanicus (Dagestan Pine Vole) 1 – Hap_7 KM656486 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2016 1 – Hap_3 KM656482 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2016 1 – Hap_20 KM656480 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 1 – Hap_2 KM656481 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 1 – Hap_4 KM656483 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 1 – Hap_1 KM656479 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 1 – Hap_6 KM656485 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 1 – Hap_5 KM656484 Adyl Su, Kabardino Balkaria, Russia Baskevich et al., 2017 2 – Hap_24 MZ198183 Kabardino Balkar, Elbruss- ky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_25 MZ198184 Kabardino Balkar, Elbruss- ky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_26 MZ198185 Kabardino Balkar, Elbruss- ky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_24 MZ198186 Kabardino Balkar, El- brussky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_27 MZ198187 Kabardino Balkar, El- brussky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_28 MZ198188 Kabardino Balkar, Elbruss- ky, Adyl Su River, Russia Bogdanov et al., 2021 2 – Hap_29 MZ198189 Kabardino Balkar, El- brussky, Adyl Su River, Russia Bogdanov et al., 2021 3 – Hap_9 KM656488 Krasnaya Polyana, Kras- nodar Krai, Russia Baskevich et al., 2017 3 – Hap_10 KM656489 Krasnaya Polyana, Kras- nodar Krai, Russia Baskevich et al., 2017 3 – Hap_11 KM656490 Krasnaya Polyana, Kras- nodar Krai, Russia Baskevich et al., 2017 3 – Hap_12 KM656491 Krasnaya Polyana, Kras- nodar Krai, Russia Baskevich et al., 2017 4 – Hap_13 MZ198175 North Ossetia Alania, Alagirsky, Nizhny Tsey Village, Russia Bogdanov et al., 2021 4 – Hap_13 MZ198176 North Ossetia Alania, Alagirsky, Nizhny Tsey Village, Russia Bogdanov et al., 2021 K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 250 C ont inue d Table 1 Map Number Collection Number Haplotype Number GenBank Accession Number Locality References 4 – Hap_14 MZ198177 North Ossetia Alania, Alagirsky, Nizhny Tsey Village, Russia Bogdanov et al., 2021 4 – Hap_15 MZ198178 North Ossetia Alania, Alagirsky, Nizhny Tsey Village, Russia Bogdanov et al., 2021 4 – Hap_32 MZ198179 North Ossetia Alania, Alagirsky, Nizhny Tsey Village, Russia Bogdanov et al., 2021 5 – Hap_21 MZ198180 Karachay Cherkess, Dom- bay Village, Gonachkhir River, Russia Bogdanov et al., 2021 5 – Hap_22 MZ198181 Karachay Cherkess, Dom- bay Village, Gonachkhir River, Russia Bogdanov et al., 2021 5 – Hap_23 MZ198182 Karachay Cherkess, Dombay Village, Go- nachkhir River, Russia Bogdanov et al., 2021 6 – Hap_18 AY513790 Beniani, Georgia Jaarola et al., 2004 7 – Hap_33 LT222300 Cew Valley, Central Caucasus, Russia Tougard, 2017 8 – Hap_8 KM656487 Nizhniy Tsei, North Ossetia, Russia Baskevich et al., 2016 9 – Hap_30 MZ198190 Kabardino Balkar, Elbruss- ky, Terskol Village, Russia Bogdanov et al., 2021 10 – Hap_31 MZ198191 Kabardino Balkar, Zolsky Ekiptsoko Russia Bogdanov et al., 2021 11 – Hap_16 AY513791 Bağdaşan, Ardahan, Türkiye Jaarola et al., 2004 12 – Hap_17 AY513792 Handere, Kars, Türkiye Jaarola et al., 2004 13 – Hap_19 MZ198174 Sarıkamış, Kars, Türkiye Bogdanov et al., 2021 14 9421 Hap_62 PX637176 Ilgar Dağı, Ardahan, Türkiye Present Study 14 9430 Hap_63 PX637177 Ilgar Dağı, Ardahan, Türkiye Present Study 14 9432 Hap_64 PX637178 Ilgar Dağı, Ardahan, Türkiye Present Study 14 9433 Hap_65 PX637179 Ilgar Dağı, Ardahan, Türkiye Present Study 15 9563 Hap_66 PX637180 Berçelan Yaylası, Hakkari, Türkiye Present Study 15 9564 Hap_67 PX637181 Berçelan Yaylası, Hakkari, Türkiye Present Study Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 251 Map Number Collection Number Haplotype Number GenBank Accession Number Locality References 15 9565 Hap_68 PX637182 Berçelan Yaylası, Hakkari, Türkiye Present Study 15 9566 Hap_69 PX637183 Berçelan Yaylası, Hakkari, Türkiye Present Study 15 9594 Hap_68 PX637184 Berçelan Yaylası, Hakkari, Türkiye Present Study 15 9595 Hap_70 PX637185 Berçelan Yaylası, Hakkari, Türkiye Present Study 16 10094 Hap_71 PX637186 Ardanuç, Artvin, Türkiye Present Study M. fingeri (Anatolian Pine Vole) 17 – Hap_34 MZ198173 Samsun, Türkiye Jaarola et al., 2004 18 – Hap_35 FR869843 Bolu, Türkiye Martínková et al. (unpubl.) 18 – Hap_36 FR869844 Bolu, Türkiye Martínková et al. (unpubl.) 19 – Hap_37 AY513836 Gümüşhane, Türkiye Jaarola et al., 2004 19 – Hap_38 FR869836 Gümüşhane, Türkiye Martínková et al. (unpubl.) 19 – Hap_39 FR869838 Gümüşhane, Türkiye Martínková et al. (unpubl.) 20 – Hap_40 FR869839 Zonguldak, Türkiye Martínková et al. (unpubl.) 20 – Hap_41 FR869840 Zonguldak, Türkiye Martínková et al. (unpubl.) 20 – Hap_42 FR869842 Zonguldak, Türkiye Martínková et al. (unpubl.) M. subterraneus (Common Pine Vole) 21 – Hap_43 AY513832 Seli, Greece Jaarola et al., 2004 22 – Hap_44 AY513833 Glocknerhaus, Austria Jaarola et al., 2004 23 – Hap_45 AY513834 Çığlıkara, Antalya, Türkiye Jaarola et al., 2004 23 – Hap_45 AY513835 Çığlıkara, Antalya, Türkiye Jaarola et al., 2004 24 – Hap_46 AJ717745 Val Piora, Ticino, Switzerland Tougard et al., 2008a, b C ont inue d Table 1 K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 252 The end Table 1 25 – Hap_47 LT222310 Úzka dolina Valley, West- ern Tatra Mts, Slovakia Tougard, 2017 26 – Hap_48 LT222311 Tourch, Finistère, France Tougard, 2017 27 – Hap_49 FR869858 Nova Kapela, Croatia Martínková et al. (unpubl.) 28 – Hap_50 FR869862 Brussels, Waterloo, Belgium Martínková et al. (unpubl.) 29 – Hap_51 FR869878 Kasperske, hory Mts, Czech Republic Martínková et al. (unpubl.) 30 – Hap_52 FR869884 Bialowieza, Poland Martínková et al. (unpubl.) 31 – Hap_53 MZ198155 Novgorod, Valdaysky, Krenye Lake, Russia Bogdanov et al., 2021 31 – Hap_54 MZ198156 Novgorod, Valdaysky, Krenye Lake, Russia Bogdanov et al., 2021 32 – Hap_55 MZ198159 Kaluga, Ulyanovsky, Nagaya Village, Russia Bogdanov et al., 2021 32 – Hap_55 MZ198160 Kaluga, Ulyanovsky, Nagaya Village, Russia Bogdanov et al., 2021 33 – Hap_56 MZ198161 Voronezh, Verkhnekhavsky, Usmanka River, Russia Bogdanov et al., 2021 33 – Hap_57 MZ198165 Voronezh, Verkhnekhavsky, Usmanka River, Russia Bogdanov et al., 2021 34 – Hap_58 MZ198169 Belgorod, Gubkinsky, Gubkin, Russia Bogdanov et al., 2021 34 – Hap_58 MZ198168 Belgorod, Gubkinsky, Gubkin, Russia Bogdanov et al., 2021 35 – Hap_59 MZ198170 Kırklareli, Türkiye Bogdanov et al., 2021 36 – Hap_60 MZ198171 Balıkesir, Türkiye Bogdanov et al., 2021 37 – Hap_61 MZ198172 Bursa, Türkiye Bogdanov et al., 2021 2003]) used as outgroups (Table 1). The final alignment included sequences with un- gapped lengths ranging from 976 to 1143 bp. Since the missing data constituted less than 5% of the total alignment, all sequences were retained without trimming, and used in subsequent phylogenetic analysis. The Maximum Likelihood (ML) phylogenetic tree was constructed in IQ-TREE v.3 (Wong et al., 2025). The best-fit nucleotide substitution models were determined by Mod- elFinder (Kalyaanamoorthy et al., 2017) implemented in IQ-TREE for both the Bayesian Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 253 Information Criterion (BIC) and the Akaike Information Criterion (AICc). Node supports were evaluated using ultrafast bootstrap (UFBoot; 3000 replicates) (Hoang et al., 2018) and the Shimodaira–Hasegawa approximate likelihood ratio test (SH-aLRT; 1000 replicates) and the approximate Bayesian support (aBayes), with the –bnni option to minimize poten- tial bootstrap overestimation. Based on the BIC, the GTR+F+I+G4 model was selected as the best-fit model for the ML analysis, whereas AICc favored GTR+F+I+R3 for Bayesian Inference (BI). Since MrBayes does not explicitly implement the “+R3” rate scheme, the Bayesian analysis was conducted under the GTR+I+G model, which represents an equiva- lent formulation using a gamma distribution with four rate categories. The BI was con- structed in MrBayes v.3.2.7 (Ronquist et al., 2020). Two independent Markov Chain Mon- te Carlo (MCMC) analyses were run, each consisting of four chains (one cold and three heated) for 10 million generations, sampling every 1,000 generations, discarding the initial 25% as burn-in. Convergence between the runs and adequate mixing were verified by en- suring that the average standard deviation of split frequencies was below 0.01 and that po- tential scale reduction factors (PSRF) approached 1.0 for all parameters. The resulting pos- terior distribution was summarized as a 50% majority-rule consensus tree, with branch lengths proportional to the mean posterior estimates. The Effective Sample Size (ESS) val- ues were evaluated in TRACER v.1.7.2 (Rambaut et al., 2018), and only parameters with ESS ≥ 200 were considered reliable. The ML and Bayesian trees were not combined into a single consensus topology. Instead, the ML tree was used as the reference, and posterior probability (PP) values obtained from the Bayesian analysis were manually added to the corresponding nodes using FigTree v.1.4.4 (Rambaut, 2018). To match the nodes, clades were compared based on their taxon composition and overall tree structure. When a node received a support value of ≥ 70 in both analyses, the two support values were shown to- gether on the same branch. If only one analysis provided support (≥ 70), the unsupported one was indicated with a (–) symbol. No changes were made to the branch structure, and no nodes were repositioned during this process. The resulting consensus trees were visual- ized, and editing PP were used to assess nodal support in FigTree v.1.4.4 software (Ram- baut, 2018). Although SH-aLRT and aBayes metrics were calculated to internally evaluate node stability, only UFBoot and Bayesian posterior probability (PP) values were added onto the final consensus tree. This approach was taken to prevent visual clutter, avoid po- tential confusion among multiple support values, and enhance the overall comprehensibil- ity of the phylogenetic relationships (Fig. 2). To examine haplotype relationships within the ‘subterraneus’ species group, cytb se- quences were analyzed using a parsimony approach. For this purpose, the TCS algorithm (Clement et al., 2000) implemented in PopART v.1.7 (Leigh & Bryant, 2015) was applied. The dataset includes both newly generated sequences (10 haplotypes of 11 samples) and the sequences obtained from GenBank (61 haplotypes among 66 samples; Table 1). M. arvalis outgroup samples were excluded from the haplotype network. The resulting network was then visualized to examine the overall genealogical structure and to assess the relative frequencies of haplotypes among lineages. Populat ion Structure Neutrality tests, including Fu and Li’s F, Fu’s Fs, Fu and Li’s D, and Tajima’s D, were performed to assess deviations from neutrality across the identified lineages. Haplo- type and nucleotide diversity indices were estimated using DnaSP v.6.12.03 (Nei & K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 254 Li, 1979; Tajima, 1989; Fu & Li, 1993; Fu, 1997; Rozas et al., 2017). Population differ- entiation was evaluated through pairwise FST values calculated in DnaSP v.6.12.03 (Rozas et al., 2017), while intra- and interspecies mean genetic distances were com- puted using the Kimura 2-parameter (K2P) model implemented in MEGA X (Ku- mar et al., 2018). Analysis was performed using the aligned cytb dataset, including all sequences used in the phylogenetic reconstruction, and analyses were performed under the pairwise deletion option to exclude gaps and ambiguous sites. Pairwise distances were computed both within M. daghestanicus (separated into Anatolian and Caucasian subclades defined by ML and Bayesian trees) and between clades/ species (M. daghestanicus, M. fingeri, and M. subterraneus). Standard deviations of mean distances were estimated through 1000 bootstrap replicates. Results Phylogenet ic Analys is The ML tree based on the mitochondrial cytb sequences from 77 individuals, with Microtus arvalis included as an outgroup, recovered the following major lineages within the ‘subterraneus’ species group of the subgenus Terricola (Fig. 2). The out- group M. arvalis (from France and Spain) was placed basally, clearly separating it from the ingroup clade comprising M. daghestanicus, M. fingeri, and M. subterra- neus. Within the ingroup, three well-supported lineages were recovered, correspond- ing to the three main species. M. daghestanicus formed a diverging lineage, sister to the clade uniting M. fingeri and M. subterraneus. The separation among these three lineages was strongly support- ed (UFBoot ≥ 94–98 across the backbone node), confirming their reciprocal mono- phyly and the robustness of the inferred topology. Two main geographic lineages with- in M. daghestanicus were identified. Sequences from the Greater Caucasus region, in- cluding localities within the Russian Federation (Kabardino-Balkaria, Karachay-Cher- kess, North Ossetia, Nizhny Tsey, Elbrussky region, Zolsky Ekiptsoko, and Cew Valley) and Georgia, formed a major geographic lineage characterized by long internal branch- es and multiple nested hierarchical splits. Within this core region, node support ranged from moderate to maximal (UFBoot = 70–100, PP = 0.71–1.0); however, a few minor internal nodes exhibited lower or unsupported UFBoot values (< 70) despite holding moderate Bayesian posterior probabilities (PP = 0.71–0.84). The Anatolian popula- tions (Ardahan, Artvin, Kars, and Hakkari), together with the western Caucasian sam- ple from Krasnaya Polyana, constituted a second subclade with moderate-to-strong support (UFBoot = 82, PP = 0.98). Within this subclade, the northeastern populations (Ardahan, Artvin, and Kars) and Krasnaya Polyana clustered into a distinct 'North' group (UFBoot = 70, PP = 0.98), standing as a sister to the Hakkari lineage with mod- erate-to-strong supported divergence (Fig. 2). The population (Berçelan Yaylası, 3324 m a. s. l.) formed a distinct peripheral branch at the southernmost limit of the species’ distribution, i.e., the northwestern end of the Zagros Mountain range, and above its known high elevation limit. This group appeared as a genetically cohesive and well-sup- ported lineage, represented by closely related haplotypes and short internal branches. The M. fingeri lineage was recovered as a monophyletic group with strong support Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 255 Fi g. 2 . C om bi ne d M L an d BI p hy lo ge ny o f t he ‘s ub te rr an eu s’ sp ec ie s g ro up (s ub ge nu s T er ric ol a) in fe rr ed fr om m ito ch on dr ia l c yt b. L ab el s a bo ve th e n od es in - di ca te M L ul tr af as t b oo ts tr ap (U FB oo t ≥ 7 0% ar e s ho w n) ; v al ue s b el ow n od es ar e B ay es ia n po st er io r p ro ba bi lit ie s ( PP ≥ 0 .7 0 ar e s ho w n) . M . a rv al is (F ra nc e an d Sp ai n) u se d as th e ou tg ro up . S ca le b ar in di ca te s s ub st itu tio ns p er si te K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 256 (UFBoot = 95, PP = 1.0). Two well-defined subclades were observed within this lineage: the first clustered the western and central Black Sea populations (Zonguldak, Bolu, and Samsun), while the second comprised the eastern Black Sea populations from Gümüşhane. Both subclades received maximal support (UFBoot = 100, PP = 1.0), in- dicating limited but geographically structured genetic divergence across northern Tür- kiye (Bogdanov et al., 2021) (Fig. 2). The M. subterraneus lineage was strongly supported (UFBoot = 98, PP = —) and displayed two well-defined geographic subdivisions. The first subclade included Eu- ropean and Balkan samples (Greece, Croatia, and Türkiye: Kırklareli, Antalya, Bursa, and Balıkesir), showing high support (UFBoot = 98–99, PP = 1.0). The second sub- clade included European populations from Austria, Switzerland, France, Slovakia, Belgium, the Czech Republic, Poland, and the Russian Federation, separated from the Anatolian–Thracian lineage with moderate support (UFBoot = 74, PP = —) (Fig. 2). The divergence between the European and Balkan-Anatolian clades sug- gests a long-term geographic isolation likely maintained since the Pleistocene glacial cycles (Jaarola et al., 2004; Abramson et al., 2021). The BI analysis based on the same cytb dataset yielded a nearly identical topology to the ML tree. Both inference methods resolved the same three major monophyletic linea- ges corresponding to M. daghestanicus, M. fingeri, and M. subterraneus. The posterior probabilities (PP ≥ 0.70) were largely congruent with the ML bootstrap values (UFBoot ≥ 70), indicating moderate to strong statistical support across principal nodes (Fig. 2). Populat ion Structure Analys is Pairwise Kimura 2-parameter (K2P) distances revealed a consistent pattern of genetic divergence among taxa within the subgenus Terricola, as summarized in Table 2. The mean divergence between the Anatolian and Caucasian lineages of M. daghestanicus was 0.0404 ± 0.0043, indicating moderate intraspecific differentiation. Genetic distances be- tween M. daghestanicus (Caucasus) and M. fingeri and M. subterraneus were 0.0955 ± 0.0085 and 0.0890 ± 0.0081, respectively, whereas the Anatolian lineage showed slightly lower divergences from the same species (0.0850 ± 0.0083 and 0.0803 ± 0.0081). The in- terspecific distance between M. fingeri and M. subterraneus averaged 0.0573 ± 0.0056. Collectively, these values support a clear genetic separation between the Anatolian and Caucasian M. daghestanicus lineages, with divergence levels lower than those observed among distinct Terricola species (Jaarola et al., 2004; Tougard, 2017; Bogdanov et al., 2021). This pattern is fully consistent with the phylogenetic tree topology and the known Table 2 . Mean Kimura 2-parameter (K2P) genetic distances based on cytb Taxon / Lineage Mean K2P distance with ± SD M. daghestanicus (Anatolia and Caucasus) 0.0404 ± 0.0043 M. daghestanicus (Anatolia) — M. fingeri 0.0850 ± 0.0083 M. daghestanicus (Caucasus) — M. fingeri 0.0955 ± 0.0085 M. daghestanicus (Anatolia) — M. subterraneus 0.0803 ± 0.0081 M. daghestanicus (Caucasus) — M. subterraneus 0.0890 ± 0.0081 M. fingeri — M. subterraneus 0.0573 ± 0.0056 ± SD: Standard Deviation. Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 257 geographical distribution of the taxa. Patterns of genetic diversity were broadly comparable across the examined line- ages within the subgenus Terricola, although the magnitude of variation differed among groups (Table 3). As expected from a wide and topographically complex dis- tribution, M. daghestanicus (Caucasus) displayed the highest nucleotide diversity (π = 0.03627) and one of the richest haplotype pools (30 haplotypes among 32 indi- viduals). This diversity was not evenly distributed; most of it was concentrated with- in the Central and Eastern Greater Caucasus, a cluster characterized by deep internal splits and an abundance of unique haplotypes — consistent with a long-term, stable population history in the eastern Greater Caucasus. In contrast, the Anatolian lineage of M. daghestanicus exhibited markedly lower nucleotide diversity (π = 0.01444), despite maintaining high haplotype richness (13 of 14 individuals). The finer subdivision within Anatolia reflected more structured dynamics: the Northeastern Anatolia (Ardahan, Artvin, and Kars) and Western Greater Caucasus (Krasnaya Polyana) showed the highest haplotype diversity (Hd = 1.000) but only moderate nucleotide diversity (0.02783), whereas the Hakkari line- age, located at the species’ southernmost limit, retained fewer haplotypes (5 of 6 in- dividuals) and the lowest nucleotide diversity (0.00658) (Table 3). This gradient — deep divergence in the Caucasus, intermediate diversity in the Northeastern Anato- lia, and shallow diversity in Hakkari — mirrors the branching pattern in the phylog- eny and the geometry of the haplotype network, where the North group forms a star-like cluster and Hakkari emerges as a compact peripheral unit (Figs 2, 3). Both M. fingeri (9 of 9 individuals) and M. subterraneus (19 of 22 individuals) Table 3 . Neutrality and genetic diversity tests for the subgenus Terricola (‘subterraneus’ species group) taxa based on cytb sequences Taxon / Lineage N h Hd π Tajima’s D Fu & Li’s D* Fu & Li’s F* M. daghestanicus (Anatolia) 14 13 0.989 0.01444 +0.234 (n.s.) −0.270 (n.s.) −0.152 (n.s.) M. daghestanicus (Caucasus) 32 30 0.996 0.03627 –1.370 (n.s.) 1.102 (n.s.) −1.416 (n.s.) M. daghestanicus (Central and Eastern Greater Caucasus) 28 26 0.995 0.02881 –1.259 (n.s.) −1.478 (n.s.) −1.661 (n.s.) M. daghestanicus (NE Anatolia and West Greater Caucasus) 12 12 1.000 0.02783 –0.843 (n.s.) −0.494 (n.s.) −0.668 (n.s.) M. daghestanicus (Northern Zagros Mnts. in Hakkari, Türkiye) 6 5 0.933 0.00658 +0.630 (n.s.) +0.342 (n.s.) +0.437 (n.s.) M. fingeri 9 9 1.000 0.02647 +0.983 (n.s.) +0.896 (n.s.) +1.031 (n.s.) M. subterraneus 22 19 0.987 0.02251 –1.195 (n.s.) −1.706 (n.s.) −1.813 (n.s.) N: Number of samples, h: Number of haplotypes, Hd: Haplotype diversity, π (pi): Nucleotide diversity, n.s., not significant at p > 0.10. K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 258 Ta bl e 4. G en et ic d iff er en tia tio n (F ST ) a m on g Te rr ic ol a (‘s ub te rr an eu s’ sp ec ie s g ro up ) ta xa b as ed o n cy tb se qu en ce s. (F ix at io n in de x; H ud so n et a l., 1 99 2) Ta xo n / L in ea ge M . d ag he sta ni - cu s ( A na to lia ) M . d ag he s- ta ni cu s ( C au - ca su s) M . d ag he sta ni cu s (C en tr al a nd Ea st er n G re at er C au ca su s) M . d ag he sta ni cu s (N E A na to lia a nd W es t G re at er C au ca su s) M . d ag he sta ni cu s (N or th er n Za gr os M nt s. in H ak ka ri, Tü rk iy e) M . fi ng er i M .su bt er ra ne us M . d ag he sta ni cu s (A na to lia ) — 0. 36 10 3 ** * 0. 44 18 3 ** * 0. 13 43 8 0. 30 27 8 * 0. 75 10 5 ** * 0. 77 62 1 ** * M . d ag he sta ni cu s (C au ca su s) 0. 36 10 3 ** * — –0 .0 16 54 0. 28 57 5 ** * 0. 46 58 5 ** * 0. 65 95 4 ** * 0. 67 36 0 ** * M . d ag he sta ni cu s (C en tr al a nd E as te rn G re at er C au ca su s) 0. 44 18 3 ** * -0 .0 16 54 — 0. 38 25 5 ** * 0. 54 37 5 ** * 0. 69 74 5 ** * 0. 71 55 9 ** * M . d ag he sta ni cu s (N E A na to lia a nd W es t G re at er C au ca su s) 0. 13 43 8 0. 28 57 5 * 0. 38 25 5 ** * — 0. 45 89 4 ** * 0. 68 99 1 ** * 0. 70 49 3 ** * M . d ag he sta ni cu s (N or th er n Za gr os M nt s. in H ak ka ri, Tü rk iy e) 0. 30 27 8 ** * 0. 46 58 5 ** * 0. 54 37 5 ** * 0. 45 89 4* — 0. 79 17 9 * 0. 81 97 0 ** * M . fi ng er i 0. 75 10 5 ** * 0. 65 95 4 ** * 0. 69 74 5 ** * 0. 68 99 1 ** * 0. 79 17 9 ** * — 0. 55 40 2 ** * M . s ub te rr an eu s 0. 77 62 1 ** * 0. 67 36 0 ** * 0. 71 55 9 ** * 0. 70 49 3 ** * 0. 81 97 0 ** * 0. 55 40 2 ** * — * 0. 01 < P < 0 .0 5; 0 .0 01 < P < 0 .0 1; * P < 0 .0 01 . Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 259 Fi g. 3 . H ap lo ty pe n et w or k co ns tr uc te d us in g th e TC S m et ho d. Th e sh ad ed a re a co lo rs fo llo w th e br an ch co lo rs in F ig . 2 K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 260 also exhibited high haplotype diversity (Hd = 1.000 and 0.987, respectively), with intermediate nucleotide diversity values, fitting their broad distributions and long- term demographic stability (Table 3). Neutrality statistics (Tajima’s D, Fu & Li’s D, and Fu & Li’s F) were non-significant across all groups, and their values fluctuated around zero. Slightly positive estimates in some lineages (e. g., M. daghestanicus (Northern Zagros Mnts. in Hakkari, Türkiye) and M. fingeri) contrast with moderately negative values in others (e. g., M. daghestanicus (the Central and Eastern Greater Caucasus) and M. subterraneus), yet none approached sta- tistical significance (Table 3). Most notably, the differences among the three M. daghestanicus sublineages — the Central and Eastern Greater Caucasus, the Northeastern Anatolia–Western Greater Cau- casus, and the southern marginal population from Hakkari located within the Zagros Mountains — are reflected more clearly in phylogenetic and network topologies than in neutrality indices, which are less sensitive to deep geographic structuring (Figs 2, 3). Pairwise FST values revealed a clear and geographically structured pattern of differen- tiation among lineages within the subgenus Terricola (Table 4). As expected for intraspecif- ic comparisons, a relatively moderate level of differentiation was observed between the Anatolian and Caucasian groups of M. daghestanicus (FST = 0.361), indicating restricted historical connectivity across the eastern Black Sea–southern Caucasus corridor. When the finer sublineages are considered, differentiation becomes more structured: the NE Anatolia and West Greater Caucasus showed moderate divergence from the Central and Eastern Greater Caucasus (FST = 0.383), whereas its separation from the Hakkari lineage was stron- ger (FST = 0.459), mirroring the phylogenetic branching order and the topology of the hap- lotype network (Figs 2, 3). The Eastern Anatolian population from Hakkari consistently displayed the highest genetic differentiation paired with clear isolation from all northern groups (FST = 0.303–0.544). These values align with the distinct peripheral placement of Hakkari haplotypes in the network and support its interpretation as a geographically isolat- ed, range-edge sublineage shaped by topographic and historical barriers (Table 4). Interspecific comparisons were markedly higher. Differentiation between M. daghes- tanicus with M. fingeri (FST = 0.660–0.792) and M. subterraneus reached (FST = 0.674– 0.820), reflecting deep and longstanding genetic separation. The contrast was strongest between M. daghestanicus (Northern Zagros Mnts. in Hakkari, Türkiye) and M. subter- raneus FST = 0.820), congruent with their pronounced mitochondrial divergence and fully non-overlapping haplotype pools. Even the closest species pair, M. fingeri and M. subterraneus, retained substantial structure (FST = 0.554), in line with previous phylo- genetic assessments (Table 4). As a result, FST values support the evolutionary scenario inferred from the phy- logenetic tree and haplotype network (Figs 2, 3, Table 4): (1) three internally coher- ent but geographically separated sublineages within M. daghestanicus, (2) limited or no gene flow at the scale of the species complex, and (3) strong species-level bound- aries among the Terricola taxa. Haplotype Network Analys is The haplotype network (Fig. 3) revealed a clear genetic structuring among the Terricola taxa. A total of 71 haplotypes among 77 individuals were identified, each forming well-delimited species-level clusters separated by several muta- Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 261 tional steps. In particular, M. fingeri and M. subterraneus formed compact, non-overlapping haplotype groups, fully consistent with the deep divergence ob- served in the ML phylogeny. Within M. daghestanicus, the northeastern Anatolian populations (Ardahan, Artvin, and Kars), together with the Western Greater Caucasian sample from Krasnaya Polyana, consistently clustered into a coherent group. This lineage dis- played a star-like configuration centered on a high-frequency haplotype (Hap_62), from which several closely related haplotypes (Hap_63–65 and Hap_71) radiated outward. GenBank sequences from Ardahan and Kars (Hap_16, Hap_17, and Hap_19) were also embedded within this cluster, reinforcing the genetic integrity of the northeastern Anatolian lineage (Fig. 3). The placement of the Krasnaya Polyana haplotypes (Hap_9–12) within this group is particularly noteworthy, revealing a pre- viously unrecognized connection between the Western Greater Caucasus and north- eastern Anatolia — a pattern not detected in earlier studies due to the absence of combined sampling from these regions (Figs 2, 3). By contrast, the southeastern Anatolian/Zagros Mnts. population (Hakkari) formed a compact peripheral cluster composed of a small number of closely related haplotypes (Hap_66–70) (Fig. 3). Although not fully star-shaped, the low internal divergence within this group points toward a potential scenario of refugial isolation or a localized founder event at the southernmost limit of the species' distribution. Discussion M. daghestanicus has a restricted distribution across the Greater and Lesser Cauca- sus in Georgia and the Russian Federation, northeastern Türkiye, Armenia, Azerbai- jan, and northwestern Iran (Kryštufek & Shenbrot, 2022). Its taxonomic placement within the genus Microtus has been repeatedly reassessed, largely due to the complex biogeographic and phylogenetic history of the ‘subterraneus’ species group (Jaarola et al., 2004; Tougard, 2017; Bogdanov et al., 2021). Our study expands this frame- work by providing new mitochondrial data from northeastern and southeastern Türkiye, thereby refining the species’ phylogeographic structure and extending its known distribution in Anatolia. A key biogeographic outcome of this work is the first confirmed record of M. da- ghestanicus from Hakkari, which represents both the southeasternmost Anatolian locality and the global southernmost range limit of the species. The occurrence of M. daghestanicus in Hakkari, localized within the Zagros orogenic belt, indicates that this lineage extends into one of the most geologically complex mountain ranges of the Middle East. The presence of M. daghestanicus at elevations of up to 3324 m a. s. l. (Berçelan Yaylası), substantially exceeds earlier records near 2900 m (Baskev- ich et al., 2017, 2021; Kryštufek & Shenbrot, 2022), and thus underscores its ecolog- ical plasticity within the montane environments. In Ardahan, Artvin, Kars, and Hak- kari, the species co-occurs with M. obscurus in alpine meadows and rocky slopes above the forest belt, offering insights into sympatric dynamics and habitat parti- tioning involving the subgenus Terricola. Both ML and Bayesian phylogenetic analyses, supported by previously publis- K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. Sözen ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 262 hed datasets (e. g., Jaarola et al., 2004; Tougard, 2017; Bogdanov et al., 2021) consis- tently resolved three major species within the ‘subterraneus’ species group — M. su- bterraneus, M. fingeri, and M. daghestanicus — with moderate to strong nodal sup- port (UFBoot ≥ 70%; PP ≥ 0.70). Within M. fingeri, the presence of geographically structured clades across the Black Sea region aligns with Bogdanov et al. (2021), who suggested possible hidden diversity. In contrast, the deep and well-supported subdi- visions within M. subterraneus are consistent with previous phylogeographic recon- structions (e. g., Jaarola et al., 2004; Baskevich et al., 2017; Bogdanov et al., 2021; Çetintürk, 2022). Our analysis also corroborates the pronounced mitochondrial structuring reported in Terricola voles (e. g., Jaarola et al., 2004; Martínková & Moravec, 2012; Baskevich et al., 2016; Bogdanov et al., 2024). Divergence values between M. daghestanicus (Anatolian and Caucasian) and M. subterraneus (8.0–8.9%) closely match estimates in Baskevich et al. (2021), while FST values ranging from 0.36 (Anatolia–Caucasus) to 0.82 (M. daghestanicus (Northern Zagros Mnts. in Hakkari, Türkiye) — M. subterraneus) clearly exceed thresholds for strong pop- ulation differentiation (Wright, 1978) (Tables 2, 4). Our results resolve three geographically coherent sublineages within M. daghes- tanicus: (i) a highly diverse Central and Eastern Greater Caucasus lineage, (ii) a Northeastern Anatolia–Western Greater Caucasus lineage, and (iii) a distinct south- eastern Anatolian/Zagros lineage in Hakkari. This structure has likely been shaped by the rugged topography of the Caucasus—Türkiye—Iran (CTI) region, where deep valleys, high mountain ridges, and habitat mosaics restrict dispersal and promote lineage divergence (Bogdanov et al., 2021). Importantly, the network and tree topol- ogies converge on the same pattern: the Caucasus core harbors long internal branch- es and high haplotype diversity, whereas northeastern Anatolia exhibits reduced di- versity and a star-like structure indicative of a relatively recent peripheral expansion (Figs 2, 3). A key finding is the placement of the Krasnaya Polyana sample in the West- ern Greater Caucasus. We show that Krasnaya Polyana clusters tightly with Arda- han, Artvin, and Kars rather than with the Central and Eastern Greater Caucasus localities. This relationship points to a shared Western-Caucasian mitochondrial ancestry and suggests that Northeastern Anatolia is genetically linked not to the Georgian populations from the Central and Eastern Greater Caucasus (e. g., Be- niani) but to the Western Greater Caucasus corridor. Similar interpretations ap- pear in Macholán et al. (2001) and Tougard (2017), who emphasized that Cauca- sus is the primary center of origin for M. daghestanicus and Terricola lineages in general. This conclusion also coincides with the previous result based on multilo- cus data showing decreasing diversity toward range margins (Bogdanov et al., 2021) and with Turkish datasets demonstrating the limited haplotype richness of Anatolian populations (Çetintürk, 2022). Taken together, our results strongly indicate that Northeastern Anatolia should not be regarded as an independent evolutionary lineage but rather as an extension of the Western Greater Caucasian mitochondrial radiation (Figs 2, 3). The identifica- tion of a distinct Hakkari lineage further highlights the role of the southeastern Anatolian mountains as biogeographic isolates along the southern fringe of the spe- Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia ISSN 2707-725X. Zoodiversity. 2026. Vol. 60, No. 3 263 cies’ distribution. The combination of phylogenetic, network, and population-genet- ic evidence underscores the CTI region as a dynamic and historically structured landscape, where elevational gradients and climatic oscillations jointly shape lineage divergence within the ‘subterraneus’ species group (Tougard, 2017; Bogdanov et al., 2021, 2024). We note that some parts of the species’ distribution remain under-sampled; therefore, broader range-wide sampling will be required to fully resolve phylogeo- graphic structure across the entire range. Notably, our sampling did not include a large portion of the known range of M. daghestanicus in the Lesser Caucasus moun- tains in Georgia and Armenia, which are geographically close to the sampled loca- tions in Ardahan, Artvin, and Kars provinces in Türkiye. It is likely that the Lesser Caucasus will show genetic similarity to the Anatolian population, but obtaining the genetic material from the remaining range of the species is necessary to complete the phylogeographic framework. Future studies integrating multilocus or SNP-based genomic datasets, wider ge- ographic sampling, and targeted investigations of potential contact zones will be es- sential to test for historical introgression and to clarify the deeper demographic his- tory of these lineages. Coupling such data with calibrated molecular clocks will allow a more precise reconstruction of divergence times and help illuminate how Pleisto- cene climatic changes and regional geomorphology contributed to the diversifica- tion of Terricola voles across the Caucasus—Türkiye—Iran region. Authors Contribution. Conceptualization, M.S. and K.K.K.; formal analysis, M.S., A.Y. and K.K.K.; investigation, M.S., F.Ç., O.Ç. and K.K.K.; writing — original draft preparation, K.K.K.; writing — review and editing, M.S., F.Ç., O.Ç., A.Y. and K.K.K.; project administration, M.S. This study forms part of K.K.K.’s PhD thesis. All authors approved the final version of the manuscript. Funding. This research was funded by the Scientific and Technological Research Council of Türkiye (TÜBİTAK, Grant Number: KBAG-123Z882) and Zonguldak Bülent Ecevit University (ZBEUN, Grant Number: 2025-84906727-02). Acknowledgements. We thank Prof. Dr. Mehmet Sait Taylan and Prof. Dr. Can Yılmaz (Hakkari Univ.) for their logistic support for accommodation and laboratory works at Hakkari University, and Necmettin Yılmaz, Kenan Çiftçi and Süleyman Dur- man (Officials of the Provincial Directorate of Nature Conservation and National Parks in Hakkari) for their guidance in the field throughout Hakkari. We also thank Kaan Tunçel for assistance with the visualizations and the reviewers for their construc- tive comments, which improved the manuscript. Conflict of interest. The authors declare no conflict of interests. Data Availability. The data supporting Table 1 of this study have been deposited and are publicly accessible in the Zenodo repository under the DOI: https://doi. org/10.5281/zenodo.20630827. Additionally, the newly generated mitochondrial cytb sequence data have been deposited in the GenBank database under accession numbers PX637176–PX637186. K. K. Kalkan, O. Çetintaş, F. Çolak, A. Yanchukov & M. 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last_indexed	2026-06-30T01:00:32Z
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spelling	oai:ojs.akademperiodyka.org.ua:article-9262026-06-29T16:20:36Z Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae) Kalkan , K. K. Çetintaş , O. Çolak , F. Yanchukov , A. Sözen , M. arvicolinae cytochrome b phylogeny small mammals Microtus daghestanicus (Shidlovskiy, 1919), one of the least studied members of the subgenus Terricola “subterraneus" species group, remains poorly understood with respect to its phylogeography and genetic structure. Here, we reevaluated its evolutionary relationships, genetic diversity and distribution of the species using mitochondrial cytb sequences (71 haplotypes of 77 samples) together with new field records from Türkiye. Maximum-likelihood and Bayesian analyses produced nearly similar topologies and separated three well-defined lineages corresponding to M. daghestanicus, M. fingeri (Neuhäuser, 1936), and M. subterraneus (Sélys, 1836). Two mitochondrial lineages were identified within M. daghestanicus: a Caucasian lineage (Russia–Georgia) and an Anatolian lineage including Ardahan, Artvin, Kars, and a newly recorded population from Hakkari. The Hakkari record represents the first verified occurrence of the species in southern part of Eastern Anatolia and marks the southern limit of the species’ known range, extending the known distribution and highlighting the Anatolia–Caucasus phylogeographic separation. Pairwise K2P distances and Fst values indicated pronounced genetic differentiation among taxa, whereas neutrality tests showed no significant deviations from mutation–drift equilibrium. Generally, observed genetic structure is consistent with long-term geographic isolation across the Pontic–Caucasian region. Our results provide a foundation for understanding the taxonomy and distribution of M. daghestanicus. Publishing House "Akademperiodyka" of the National Academy of Sciences of Ukraine 2026-04-27 Article Article application/pdf https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/926 10.15407/zoo2026.03.245 Zoodiversity; Vol. 60 No. 3 (2026): Zoodiversity Zoodiversity (Vestnik Zoologii); Том 60 № 3 (2026): Zoodiversity 2707-7268 2707-725X 10.15407/zoo2026.03 en https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/926/396 Copyright (c) 2026 K. K. Kalkan , O. Çetintaş , F. Çolak , A. Yanchukov , M. Sözen
spellingShingle	Kalkan , K. K. Çetintaş , O. Çolak , F. Yanchukov , A. Sözen , M. Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title	Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title_full	Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title_fullStr	Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title_full_unstemmed	Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title_short	Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)
title_sort	phylogeography of terricola voles in the caucasus and eastern anatolia, with a new southernmost record of microtus daghestanicus (rodentia, cricetidae, arvicolinae)
topic_facet	arvicolinae cytochrome b phylogeny small mammals
url	https://ojs.akademperiodyka.org.ua/index.php/Zoodiversity/article/view/926
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Phylogeography of Terricola Voles in the Caucasus and Eastern Anatolia, with a New Southernmost Record of Microtus daghestanicus (Rodentia, Cricetidae, Arvicolinae)

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