Populations of Transcarpathia and Bukovina on the genetic landscape of surrounding regions

O. M. Utevska, M. I. Chukhraeva, A. T. Agdzhoyan, L. A. Atramentova, E. V. Balanovska, O. P. Balanovsky

Abstract


The territory of present-day Ukraine is subdivided into some regions with specific demographic and politic history. Nevertheless, the corresponding subdivision in genetic structure is not revealed in previous investigations: populations of Ukrainians under study were genetically homogeneous on SNP markers of Y chromosome. In the current investigation we studied the Y-chromosomal genetic structure of Transcarpathia and Bukovina populations. Several factors exist to expect the genetic specificity of these populations. Both ones are placed in the Carpathian foothills, at the south-western border of the Ukrainian area. During the last millennium these territories were the parts of different states and were open for ethnically diverse migrations. It was revealed that the major Y chromosomal haplogroups in Transcarpathia population were R1a1a1*(М198), I2a (Р37.2), R1a1a1g (М458), E1b1b1a1 (M78). The major haplogroups in Bukovina population were I2a (Р37.2), R1a1a1*(М198), R1a1a1g (М458), R1b1b2 (М269), E1b1b1a1 (M78), I1 (М253). The Bukovina population differs from the typical Ukrainian population by higher frequency of I2a (Р37.2) and lower frequency of R1a1a1*(М198). Moreover, this is the only population among ones studied in Ukraine where the most frequent haplogroup is I2a (Р37.2) but not R1a1a1*(М198). Such a deviation can be caused by possible mixing with neighbouring southern groups, and Carpathian mountains were not a border for exchange in this case. Interestingly, the haplogroup N1c (M178) is not revealed in Transcarpathia at all, obviously due to the mountain barrier. It was revealed by principal component analysis that Ukrainians from Transcarpathia and Bukovina despite some specific peculiarities are more similar to other Ukrainian populations than to the surrounding ethnic groups such as Poles, Slovaks, Hungarians, Romanians, Moldavians and Gagauzes. Ukrainians of Transcarpathia and Bukovina form the entire genetic continuum with the whole Ukraine on maps of gene distances, confirming the homogeneity of Ukrainian parental gene pool and it’s differentiation from other groups. After performing the analysis of Y-haplogroup spatial distribution, it is supposed that the northern ridges ofCarpathian mountainsare the East-European barrier decreasing the gene flow. It decreases the spreading of haplogroups N1c (М178) and R1a (М198) southward and movement of E1b (М78), R1b (М269), J (М304) and G (М201) northward. 


Keywords


Ukrainians; SNP markers; Y chromosome; haplogroups; Nei distances

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References


Balanovsky, O., Dibirova, K., Dybo, A., Mudrak, O., Frolova, S., Pocheshkhova, E., Haber, M., Platt, D., Schurr, T., Haak, W., Kuznetsova, M., Radzhabov, M., Balaganskaya, O., Druzhinina, E., Zakharova, T., Hernanz, D., Zalloua, P., Koshel, S., Ruhlen, M., Renfrew, C., Wells, R.S., Tyler-Smith, C., Balanovska, E., The Genographic Consortium., 2011. Parallel evolution of genes and languages in the Caucasus region. Mol. Biol. Evol. 28(10), 2905–2920. >> doi: 10.1093/molbev/msr126

Balanovsky, O., Rootsi, S., Pshenichnov, A., Kivisild, T., Churnosov, M., Evseeva, I., Pocheshkhova, E., Boldyreva, M., Yankovsky, N., Balanovska, E., Villems, R., 2008. Two sources of the Russian patrilineal heritage in their Eurasian context. Am. J. Hum. Genet. 82(1), 236–250. >> doi: 10.1016/j.ajhg.2007.09.019

Barbujani, G., Bertorelle, G., 2001. Genetics and the population history of Europe. Proc. Natl. Acad. Sci. USA 98(1), 22–25. >> doi: 10.1073/pnas.98.1.22

Battaglia, V., Fornarino, S., Al-Zahery, N., Olivieri, A., Pala, M., Myres, N.M., King, R.J., Rootsi, S., Marjanovic, D., Primorac, D., Hadziselimovic, R., Vidovic, S., Drobnic, K., Durmishi, N., Torroni, A., Santachiara-Benerecetti, A.S., Underhill, P.A., Semino, O., 2009. Y-chromosomal evidence of the cultural diffusion of agriculture in Southeast Europe. Eur. J. Hum. Genet. 17(6), 820–830. >> doi: 10.1038/ejhg.2008.249

Chiaroni, J., Underhill, P., Cavalli-Sforza, L.L., 2009. Y chromosome diversity, human expansion, drift, and cultural evolution. Proc. Natl. Acad. Sci. 106(48), 20174–20179. >> doi: 10.1073/pnas.0910803106

Cruciani, F., La Fratta, R., Trombetta, B., Santolamazza, P., Sellitto, D., Colomb, E.B., Dugoujon, J.M., Crivellaro, F., Benincasa, T., Pascone, R., Moral, P., Watson, E., Melegh, B., Barbujani, G., Fuselli, S., Vona, G., Zagradisnik, B., Assum, G., Brdicka, R., Kozlov, A.I., Efremov, G.D., Coppa, A., Novelletto, A., Scozzari, R., 2007. Tracing past human male movements in northern/eastern Africa and western Eurasia: New clues from Y-chromosomal haplogroups E-M78 and J-M12. Mol. Biol. Evol. 24(6), 1300–1311. >> doi: 10.1093/molbev/msm049

Har’kov, V.N., Stepanov, V.A., Borinskaja, S.A., Kozhekbaeva, Z.M., Gusar, V.A., Grechanina, E.J., Puzyrev, V.P., Husnutdinova, J.K., Jankovskij, N.K., 2004. Struktura genofonda vostochnyh ukraincev po gaplogruppam Y-hromosomy [The gene pool structure of Eastern Ukrainians on Y chromosome haplogroups]. Genetika 40(3), 415–421 (in Russian).

Jobling, M., Tyler-Smith, C., 2003. The human Y chromosome: An evolutionary marker comes of age. Nat. Rev. Genet. 4, 598–612. >> doi: 10.1038/nrg1124

Karafet, T.M., Mendez, F.L., Meilerman, M.B., Underhill, P.A., Zegura, S.L., Hammer, M.F., 2008. New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res. 18, 830–838. >> doi: 10.1101/gr.7172008

Kayser, M., Lao, O., Anslinger, K., Augustin, C., Bargel, G., Edelmann, J., Elias, S., Heinrich, M., Henke, J., Henke, L., Hohoff, C., Illing, A., Jonkisz, A., Kuzniar, P., Lebioda, A., Lessig, R., Lewicki, S., Maciejewska, A., Monies, DM., Pawłowski, R., Poetsch, M., Schmid, D., Schmidt, U., Schneider, P.M., Stradmann-Bellinghausen, B., Szibor, R., Wegener, R., Wozniak, M., Zoledziewska, M., Roewer, L., Dobosz, T., Ploski, R., 2005. Significant genetic differentiation between Poland and Germany follows present-day political borders, as revealed by Y-chromosome analysis. Hum Genet. 117, 428–443. >> doi: 10.1007/s00439-005-1333-9

Koshel, S., 2012. Geoinformation technologies in genegeography. In: Mod. Geogr. Cartogr. Artic. Collect. Ed. Lure, I.K., Kravtsova, V.I., 158–166.

Kushniarevich, A., Utevska, O., Chuhryaeva, M., Agdzhoyan, A., Dibirova, K., Uktveryte, I., Möls, M., Mulahasanovic, L., Pshenichnov, A., Frolova, S., Shanko, A., Metspalu, E., Reidla, M., Tambets, K., Tamm, E., Koshel, S., Zaporozhchenko, V., Atramentova, L., Kučinskas, V., Davydenko, O., Goncharova, O., Evseeva, I., Churnosov, M., Pocheshchova, E., Yunusbayev, B., Khusnutdinova, E., Marjanović, D., Rudan, P., Rootsi, S., Yankovsky, N., Endicott, P., Kassian, A., Dybo, A., Genographic Consortium, Tyler-Smith, C., Balanovska, E., Metspalu, M., Kivisild, T., Villems, R., Balanovsky, O., 2015. Genetic heritage of the Balto-Slavic speaking populations: A synthesis of autosomal, mitochondrial and Y-chromosomal data. PLoS One 10(9), e0135820. >> doi: 10.1371/journal.pone.0135820

Lappalainen, T., Laitinen, V., Salmela, E., Andersen, P., Huoponen, K., Savontaus, M.L., Lahermo, P., 2008. Migration waves to the Baltic sea region. Ann. Hum. Genet. 72(3), 337–348. >> doi: 10.1111/j.1469-1809.2007.00429.x

Mielnik-Sikorska, M., Daca, P., Woźniak, M., Malyarchuk, B.A., Bednarek, J., Dobosz, T., Grzybowski, T., 2013. Genetic data from Y chromosome STR and SNP loci in Ukrainian population. Forensic Sci. Int. Genet. 7(1), 200–203. >> doi: 10.1016/j.fsigen.2012.05.007

Myres, N.M., Rootsi, S., Lin, A.A., Järve, M., King, R.J., Kutuev, I., Cabrera, V.M., Khusnutdinova, E.K., Pshenichnov, A., Yunusbayev, B., Balanovsky, O., Balanovska, E., Rudan, P., Baldovic, M., Herrera, R.J., Chiaroni, J., Di Cristofaro, J., Villems, R., Kivisild, T., Underhill, P.A., 2011. A major Y-chromosome haplogroup R1b Holocene era founder effect in Central and Western Europe. Eur. J. Hum. Genet. 19(1), 95–101. >> doi: 10.1038/ejhg.2010.146

Nei, M., 1972. Genetic distance between populations. Am Nat. 106, 283–292. >> doi: 10.1086/282771

Novelletto, A., 2007. Y chromosome variation in Europe: Continental and local processes in the formation of the extant gene pool. Ann. Hum. Biol. 34(2), 139–172. >> doi: 10.1080/03014460701206843

Pericić, M., Lauc, L.B., Klarić, I.M., Rootsi, S., Janićijevic, B., Rudan, I., Terzić, R., Colak, I., Kvesić, A., Popović, D., Sijacki, A., Behluli, I., Dordevic, D., Efremovska, L., Bajec, D.D., Stefanović, B.D., Villems, R., Rudan, P., 2005. High-resolution phylogenetic analysis of southeastern Europe traces major episodes of paternal gene flow among Slavic populations. Mol. Biol. Evol. 22, 1964–1975. >> doi: 10.1093/molbev/msi185

Rębała, K., Martínez-Cruz, B., Tönjes, A., Kovacs, P., Stumvoll, M., Lindner, I., Büttner, A., Wichmann, H.E., Siváková, D., Soták, M., Quintana-Murci, L., Szczerkowska, Z., Comas, D., Genographic Consortium. 2013. Contemporary paternal genetic landscape of Polish and German populations: From early medieval Slavic expansion to post-World War II resettlements. Eur. J. Hum. Genet. 21, 415–422.

Rootsi, S., Myres, N.M., Lin, A.A., Järve, M, King, R.J., Kutuev, I., Cabrera, V.M., Khusnutdinova, E.K., Varendi, K., Sahakyan, H., Behar, D.M., Khusainova, R., Balanovsky, O., Balanovska, E., Rudan, P., Yepiskoposyan, L., Bahmanimehr, A., Farjadian, S., Kushniarevich, A., Herrera, R.J., Grugni, V., Battaglia, V., Nici, C., Crobu, F., Karachanak, S., Kashani, B.H., Houshmand, M., Sanati, M.H., Toncheva, D., Lisa, A., Semino, O., Chiaroni, J., Cristofaro, J.D., Villems, R., Kivisild, T., Underhill, P.A., 2012. Distinguishing the co-ancestries of haplogroup G Y-chromosomes in the populations of Europe and the Caucasus. Eur. J. Hum. Genet. 20(12), 1275–1282. >> doi: 10.1038/ejhg.2012.86

Rootsi, S., Zhivotovsky, L.A., Baldovic, M., Kayser, M., Kutuev, I.A., Khusainova, R., Bermisheva, M.A., Gubina, M., Fedorova, S.A., Ilumäe, A.M., Khusnutdinova, E.K., Voevoda, M.I., Osipova, L.P., Stoneking, M., Lin, A.A., Ferak, V., Parik, J., Kivisild, T., Underhill, P.A., Villems, R., 2007. A counter-clockwise northern route of the Y-chromosome haplogroup N from Southeast Asia towards Europe. Eur. J. Hum. Genet. 15(2), 204–211. >> 10.1038/sj.ejhg.5201748

Underhill, P.A., Myres, N.M., Rootsi, S., Chow, C.T., Lin, A.A., Otillar, R.P., King, R., Zhivotovsky, L.A., Balanovsky, O., Pshenichnov, A., Ritchie, K.H., Cavalli-Sforza, L.L., Kivisild, T., Villems, R., Woodward, S.R., 2007. New phylogenetic relationships for Y-chromosome haplogroup I: Reappraising its phylogeography and prehistory. In: Mellars, P., Boyle, K., Bar-Yosef, O., Stringer, C. (Eds). Rethinking the human revolution. McDonald Institute for Archaeological Research, Cambridge, UK. 33–42.

Underhill, P.A., Myres, N.M., Rootsi, S., Metspalu, M., Zhivotovsky, L.A., King, R.J., Lin, A.A., Chow, C.E., Semino, O., Battaglia, V., Kutuev, I., Järve, M., Chaubey, G., Ayub, Q., Mohyuddin, A., Mehdi, S.Q., Sengupta, S., Rogaev, E.I., Khusnutdinova, E.K., Pshenichnov, A., Balanovsky, O., Balanovska, E., Jeran, N., Augustin, D.H., Baldovic, M., Herrera, R.J., Thangaraj, K., Singh, V., Singh, L., Majumder, P., Rudan, P., Primorac, D., Villems, R., Kivisild, T., 2010. Separating the post-Glacial coancestry of European and Asian Y chromosomes within haplogroup R1a. Eur. J. Hum. Genet. 18(4), 479–484. >> doi: 10.1038/ejhg.2009.194

Underhill, P.A., Passarino, G., Lin, A.A., Shen, P., Mirazon, L.M., Foley, R.A., Oefner, P.J., Cavalli-Sforza, L.L., 2001. The phylogeography of Y chromosome binary haplotypes and the origins of modern human рopulations. Ann. Hum. Genet. 65, 43–62.

Utevska, O.M., Agdzhojan, A.T., Balanovska, E.V., Atramentova, L.A., Balanovsky, O.P., 2013. Istoki formirovanija ukrainskogo genofonda po dannym ob Y-hromosome [The origin of Ukrainian gene pool on Y-chromosomal data]. Vіsnik Harkіvs'kogo unіversitetu 18(1079), 87–98 (in Russian).

Utevska, O.M., Agdzhojan, A.T., Pshenichnov, A.S., Dibirova, H.D., Chuhrjaeva, M.I., Atramentova, L.A., Balanovska, E.V., Balanovsky, O.P., 2013. Shodstvo ukrainskih populjacij iz razlichnyh territorial'nyh podrazdelenij po markeram Y-hromosomy. [Similarity of Ukrainian populations from different regions revealed by Y-chromosomal markers]. Faktory Jeksperimental'noj Jevoljucii Organizmov. Logos, Kiev. 338–341 (in Russian).

Utevska, O.M., Pshenichnov, A.S., Dibirova, H.D., Rootsi, S., Agdzhojan, A.T., Churnosov, M.I., Balanovska, E.V., Atramentova, L.A., Balanovsky, O.P., 2015. Shodstvo i razlichija genofondov ukrainskih i russkih populjacij Slobozhanshhiny po markeram Y-hromosomy [Gene pool similarities and differences between Ukrainians and Russians of Slobozhanshina on Y-chromosome data]. Citologija i Genetika 49(4), 40–50 (in Russian).

Varzari, A., Kharkov, V., Simonova, K., Stepanov, V., Stephan, W., Weiss, E.H., Nikitin, A.G., Raicu, F., 2013. Paleo-Balkan and Slavic contributions to the genetic pool of Moldavians: Insights from the Y chromosome. PLoS One 8(1), e53731. >> doi: 10.1371/journal.pone.0053731

Völgyi, A., Zalán, A., Szvetnik, E., Pamjav, H., 2009. Hungarian population data for 11 Y-STR and 49 Y-SNP markers. Forensic Sci. Int. Genet. 3(2), e27-8. >> doi: 10.1016/j.fsigen.2008.04.006

Woźniak, M., Malyarchuk, B., Derenko, M., Vanecek, T., Lazur, J., Gomolcak, P., Grzybowski, T., 2010. Similarities and distinctions in Y chromosome gene pool of Western Slavs. Am. J. Phys. Anthropol. 142(4), 540–548. >> 10.1002/ajpa.21253

Y-Chromosome Concortium, 2002. A nomenclature system for the tree of human Y-chromosomal binary haplogroups. Genome Res. 12, 339–348.

Yunusbayev, B., Metspalu, M., Järve, M., Kutuev, I., Rootsi, S., Metspalu, E., Behar, D.M., Varendi, K., Sahakyan, H., Khusainova, R., Yepiskoposyan, L., Khusnutdinova, E.K., Underhill, P.A., Kivisild, T., Villems, R., 2012. The Caucasus as an asymmetric semipermeable barrier to ancient human migrations. Mol. Biol. Evol. 29(1), 359–365. >> doi: 10.1093/molbev/msr221




DOI: http://dx.doi.org/10.15421/021524

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