Abstract
The stone marten (Martes foina) is a small carnivore distributed from Europe to Central Asia. To investigate its phylogeography, we sequenced part of the mitochondrial control-region (485 bp) for 30 individuals from 26 localities broadly covering the species range across continental Eurasia. We identified 16 haplotypes, which comprised two major groups along with the previously reported haplotypes: the Major Eurasian group that included haplotypes widely distributed from Europe to Central Asia, and the Eastern Turkey group containing haplotypes restricted to eastern Turkey. Our phylogeographic and demographic analyses indicated a recent population expansion for the Major Eurasian group, but no clear evidence for the Eastern Turkey group. Our results also suggested that the refugial M. foina population on the Balkan Peninsula expanded to Western Turkey, most of Europe, and Central Asia since the Last Glacial Maximum due to the lack of significant geographical barriers, although the small number of samples limits our understanding of the overall phylogeography. On the other hand, this assumption does not exclude the possibility that some of the central Asian populations in the Major Eurasian group could have originated from somewhere in central Asia.
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Data availability
The nucleotide sequences obtained in the present study will appear at the DNA Data Bank of Japan (DDBJ: https://www.ddbj.nig.ac.jp/index-e.html) with accession nos. LC663748–LC663762.
References
Abramov AV, Kranz A, Herrero J, Choudhury A, Maran T (2016) Martes foina. The IUCN Red List of Threatened Species 2016:e.T29672A45202514
Anderson E (1970) Quaternary evolution of the genus Martes (Carnivora, Mustelidae). Acta Zool Fenn 130:1–132
Arslan Y, Demirtaş S, Herman JS, Pustilnik JD, Searle JB, Gündüz İ (2020) The Anatolian glacial refugium and human-mediated colonization: a phylogeographical study of the stone marten (Martes foina) in Turkey. Biol J Linn Soc 129:470–491. https://doi.org/10.1093/biolinnean/blz180
Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Baryshnikov GF (2009) Pleistocene Mustelidae (Carnivora) from Paleolithic site in Kudaro caves in the Caucasus. Russ J Theriol 8:75–95 https://doi.org/10.15298/rusjtheriol.08.2.02
Basto MP, Reis MS, Simões L, Grilo C, Cardoso L, Cortes H, Bruford MW, Fernandes C (2016) Assessing genetic structure in common but ecologically distinct carnivores: the Stone marten and red Fox. PLoS ONE 11:e0145165. https://doi.org/10.1371/journal.pone.0145165
Dawson NG, Hope AG, Talbot SL, Cook JA (2014) A multilocus evaluation of ermine (Mustela erminea) across the Holarctic, testing hypotheses of Pleistocene diversification in response to climate change. J Biogeography 41:464–475. https://doi.org/10.1111/jbi.12221
De Marinis AM, Pandolfi M (1995) Morphometric variation in stone marten Martes Foina in western Alps in relation to climate. Italian J Mamm 7:119–125. https://doi.org/10.4404/hystrix-7.1-2-4060
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resource 10:564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fu XY (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking, and background selection. Genetics 147:915–925. https://doi.org/10.1093/genetics/147.2.915
Ghaedi Z, Badri S, Pirooz RS, Vaissi S, Javidkar M, Ahmadzadeh F (2021) The Zagros Mountains acting as a natural barrier to gene flow in the Middle East: more evidence from the evolutionary history of spiny-tailed lizards (Uromasticinae: Saara). Zool J Linn Soc 192:1123–1136. https://doi.org/10.1093/zoolinnean/zlaa113
Hirata D, Abramov AV, Baryshnikov GF, Masuda R (2014) Mitochondrial DNA haplogrouping of the brown bear, Ursus arctos (Carnivora: Ursidae) in Asia, based on a newly developed APLP analysis. Biol J Linn Soc 111:627–635. https://doi.org/10.1111/bij.12219
İbiş O, Koepfli KP, Özcan S, Tez C (2018) Genetic analysis of Turkish martens: Do two species of the genus Martesoccur in Anatolia? Zool Scripta 47:390–403. https://doi.org/10.1111/zsc.12289
Ishikawa K, Abramov AV, Amaike Y, Nishita Y, Masuda R (2020) Phylogeography of the Siberian weasel (Mustela sibirica), based on a mitochondrial DNA analysis. Biol J Linn Soc 129:587–593. https://doi.org/10.1093/biolinnean/blz202
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kurose N, Abramov AV, Masuda R (2005) Comparative phylogeography between the ermine Mustela erminea and the least weasel M. nivalis of Palaearctic and Nearctic regions, based on analysis of mitochondrial DNA control region sequences. Zool Sci 22:1069–1078. https://doi.org/10.2108/zsj.22.1069
Kurten B (1968) Pleistocene Mammals of Europe. Weidenfeld & Nicolson, London
Kutschera VE, Lecomte N, Janke A, Selva N, Sokolov AA, Haun T, Steyer K, Nowak C, Hailer F (2013) A range-wide synthesis and timeline for phylogeographic events in the red fox (Vulpes vulpes). BMC Evol Biol 13:114. https://doi.org/10.1186/1471-2148-13-114
Llorente-Rodriguez L, Nores-Quesada C, Lopez-Saez JA, Morales-Muniz A (2016) Hidden signatures of the Mesolithic-Neolithic transition in Iberia: the pine marten (Martes martes Linnaeus, 1758) and beech marten (Martes foina Erxleben, 1777) from Cova Fosca (Spain). Quat Internat 403:174–186. https://doi.org/10.1016/j.quaint.2015.05.046
Masuda R, Amano T, Ono H (2001) Ancient DNA analysis of brown bear (Ursus arctos) remains from the archeological site of Rebun Island, Hokkaido, Japan. Zool Sci 18:741–751. https://doi.org/10.2108/zsj.18.741
Nagai T, Raichev EG, Tsunoda H, Kaneko Y, Masuda R (2012) Preliminary study on microsatellite and mitochondrial DNA variation of the stone marten Martes foina in Bulgaria. Mammal Study 37:353–358. https://doi.org/10.3106/041.037.0410
Papakosta M (2017) Biometric variation in Martes foina from mainland Greece and the Aegean Islands. Turkish J Zool 41:654–663. https://doi.org/10.3906/zoo-1612-8
Proulx G, Aubry K, Birks J, Buskirk S, Fortin C, Frost H, Krohn W, Mayo L, Monakhov V, Payer D, Saeki M, Santos-Reis M, Weir R, Zielinski W (2004) World distribution and status of the genus Martes in 2000. In: Harrison DJ, Fuller AK, Proulx G (eds) Martens and Fishers (Martes) in Human-altered Environments: An International Perspective. Springer, New York, 21–76
Reig S (1992) Geographic variation in pine marten (Martes martes) and beech marten (Martes foina) in Europe. J Mamm 73:744–769. https://doi.org/10.2307/1382193
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302. https://doi.org/10.1093/molbev/msx248
Ruiz-González A, Madeira MJ, Randi E, Abramov AV, Davoli F, Gómez-Moliner BJ (2013) Phylogeography of the forest-dwelling European pine marten (Martes martes): new insights into cryptic northern glacial refugia. Biol J Linn Soc 109:1–18. https://doi.org/10.1111/bij.12046
Sato T, Abramov AV, Raichev EG, Kosintsev PA, Väinölä R, Murakami T, Kaneko Y, Masuda R (2020) Phylogeography and population history of the least weasel (Mustela nivalis) in the Palearctic, based on multilocus analysis. J Zool System Evol Res 58:408–426. https://doi.org/10.1111/jzs.12330
Sommer R, Benecke N (2004) Late- and post-glacial history of the Mustelidae in Europe. Mamm Rev 34:249–284. https://doi.org/10.1111/j.1365-2907.2004.00043.x
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595. https://doi.org/10.1093/genetics/123.3.585
Tsoupas A, Andreadou M, Papakosta MA, Karaiskou N, Bakaloudis DE, Chatzinikos E, Sakoulis A, Triantafyllidis A, Vlachos CG (2019) Phylogeography of Martes foina in Greece. Mamm Biol 95:59–68. https://doi.org/10.1016/j.mambio.2019.02.004
Vergara M, Basto MP, Madeira MJ, Gómez-Moliner BJ, Santos-Reis M, Fernandes C, Ruiz-González A (2015) Inferring population genetic structure in widely and continuously distributed carnivores: the stone marten (Martes foina) as a case study. PLoS ONE 10:e0134257 https://doi.org/10.1371/journal.pone.0134257
Wereszczuk A, Leblois R, Zalewski A (2017) Genetic diversity and structure related to expansion history and habitat isolation: stone marten populating rural-urban habitats. BMC Ecol 17:46. https://doi.org/10.1186/s12898-017-0156-6
Zigouris J, Schaefer JA, Fortin C, Kyle CJ (2013) Phylogeography and postglacial recolonization in wolverines (Gulo gulo) from across their circumpolar distribution. PLoS ONE 8:e83837. https://doi.org/10.1371/journal.pone.0083837
Acknowledgements
We thank Dr. Matthew H. Dick for commenting on the manuscript and editing our English.
Funding
This study was supported in part by the Japan-Russia Research Cooperative Program between the Japan Society for the Promotion of Science (JSPS; No. JPJSBP120194802) and the Russian Foundation of Basic Research (RFBR); a Joint Research Program grant from the Japan Arctic Research Network Center; and by the Ministry of Science and Higher Education of the Russian Federation (No. 075–15-2021–1069).
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Ishii, H., Amaike, Y., Nishita, Y. et al. Phylogeography of the stone marten (Martes foina: Mustelidae: Mammalia) in Eurasia, based on a mitochondrial DNA analysis. Mamm Res 68, 375–381 (2023). https://doi.org/10.1007/s13364-023-00690-6
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DOI: https://doi.org/10.1007/s13364-023-00690-6