Abstract
Populations of northeastern Europe and the Uralic mountain range are found in close geographic proximity, but they have been subject to different demographic histories. The current study attempts to better understand the genetic paternal relationships of ethnic groups residing in these regions. We have performed high-resolution haplotyping of 236 Y-chromosomes from populations in northwestern Russia and the Uralic mountains, and compared them to relevant previously published data. Haplotype variation and age estimation analyses using 15 Y-STR loci were conducted for samples within the N1b, N1c1 and R1a1 single-nucleotide polymorphism backgrounds. Our results suggest that although most genetic relationships throughout Eurasia are dependent on geographic proximity, members of the Uralic and Slavic linguistic families and subfamilies, yield significant correlations at both levels of comparison making it difficult to denote either linguistics or geographic proximity as the basis for their genetic substrata. Expansion times for haplogroup R1a1 date approximately to 18 000 YBP, and age estimates along with Network topology of populations found at opposite poles of its range (Eastern Europe and South Asia) indicate that two separate haplotypic foci exist within this haplogroup. Data based on haplogroup N1b challenge earlier findings and suggest that the mutation may have occurred in the Uralic range rather than in Siberia and much earlier than has been proposed (12.9±4.1 instead of 5.2±2.7 kya). In addition, age and variance estimates for haplogroup N1c1 suggest that populations from the western Urals may have been genetically influenced by a dispersal from northeastern Europe (eg, eastern Slavs) rather than the converse.
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References
Pavlov P, Roebroeks W, Svedsen JI : The Pleistocene colonization of northeastern Europe: a report on recent research. J Hum Evol 2004; 47: 3–17.
Otte M : The northwestern European Plain around 18 000 BP; In Soffer O, Gamble C (eds): The World at 18 000 BP. Unwin Hyman: London, 1990, Vol 1, pp 54–68.
Torroni A, Bandelt H, D’Urbano L et al: mtDNA analysis reveals a major late Paleolithic population expansion from southwestern to northeastern Europe. Am J Hum Genet 1998; 62: 1137–1152.
Lappalainen T, Koivumaki S, Salmela E, Huoponen K, Sistonen P, Savontaus ML, Lahermo P : Regional differences among the Finns: a Y-chromosomal perspective. Gene 2006; 376: 207–215.
Simchenko YuB : Early ethnogenesis of ethnic groups of the Ural language family from transpolar and circumpolar Eurasia; In Gurvich IS (ed): Ethnogenez narodov severa. Moscow: Nauka, 1980, pp 11–27.
Sajantila A, Lahermo P, Anttinen T et al: Genes and languages in Europe: an analysis of mitochondrial lineages. Genome Res 1995; 5: 42–52.
Malyarchuk BA : Differentiation of the mitochondrial subhaplogroup U4 in the populations of Eastern Europe, Ural, and Western Siberia: implication to the genetic history of the Uralic populations. Genetika 2004; 40: 1281–1287.
Verbenko DA, Knjazev AN, Mikulich AI, Khusnutdinova EK, Bebyakova NA, Limborska SA : Variability of the 3′APOB minisatellite locus in eastern Slavonic populations. Hum Hered 2005; 60: 10–18.
Verbenko DA, Slominsky PA, Spitsyn VA et al: Polymorphisms at locus D1S80 and other hypervariable regions in the analysis of Eastern European ethnic group relationships. Ann Hum Biol 2006; 33: 570–584.
Khrunin A, Verbenko D, Nikitina K, Limborska S : Regional differences in the genetic variability of Finno-Ugric speaking Komi populations. Am J Hum Bio 2007; 19: 741–750.
Khrunin AV, Tarskaia LA, Spitsyn VA, Lylova OI, Bebyakova NA, Mikulich AI, Limborska SA : p53 polymorphisms in Russia and Belarus: correlation of the 2-1-1 haplotype frequency with longitude. Mol Genet Genomics 2005; 272: 666–672.
Wells RS, Yuldasheva N, Ruzibakiev R et al: The Eurasian heartland: a continental perspective on Y-chromosomal diversity. Proc Natl Acad USA 2001; 98: 10244–10249.
Semino O, Passarino G, Oefner PJ et al: The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: A Y chromosome perspective. Science 2000; 290: 1155–1159.
Zerjal T, Dashnyam B, Pandya A et al: Genetic relationships of Asians and Northern Europeans, revealed by Y-chromosomal DNA analysis. Am J Hum Genet 1997; 60: 1174–1183.
Rootsi S, Zhivotovsky LA, Baldovic M et al: A counter-clockwise northern route of the Y-chromosome haplogroup N from Southeast Asia towards Europe. Eur J Hum Genet 2007; 15: 211–405.
Xue Y, Zerjal T, Ban W et al: Male demography in East Asia: a north–south contrast in human population expansion times. Genetics 2006; 172: 2431–2439.
Guglielmino CR, Piazza A, Menozzi P, Cavalli-Sforza LL : Uralic genes in Europe. Am J Phys Anthropol 1990; 83: 57–68.
Sengupta S, Zhivotovsky LA, King R et al: Polarity and temporality of high-resolution Y-chromosome distributions in India identify both indigenous and exogenous expansions and reveals minor genetic influence of Central Asian pastoralists. Am J Hum Genet 2006; 78: 202–221.
Niitemaa V, Hovi K : Baltian Historia (Jyväskylä). Helsinki, Finland, 1991, pp 272–276.
Harvey RG, Tills D, Warlow A et al: Genetic affinities of the Balts. A study of blood groups, serum proteins and enzymes of Lithuanians in the United Kingdom. Man (N. S.) 1983; 18: 535–552.
Rudiger L, Edelmann J : Population data of Y-chromosomal STRs in Lithuanian, Latvian and Estonian males. Forensic Sci Int 2001; 120: 223–225.
Rebala K, Mikulich AI, Tsybovsky IS et al: Y-STR variation among Slavs: evidence for the Slavic homeland in the Middle Dnieper Basin. J Hum Genet 2007; 52: 406–414.
Balanovsky O, Rootsi S, Pshenichnov A et al: Two sources of the Russian patrilineal heritage in their Eurasian context. Am J of Hum Genet 2008; 82: 236–250.
Malyarchuk BA, Grzybowski T, Derenko MV et al: Mitochondrial DNA variability in Poles and Russians. Ann Hum Genet 2002; 66: 261–283.
Belyaeva O, Bermisheva M, Khrunin A et al: Mitochondrial DNA variations in Russian and Belorussian populations. Hum Biol 2003; 75: 647–660.
Khar’kov VN, Stepanov VA, Borinskaya SA et al: Gene pool structure of Eastern Ukrainians as inferred from the Y-chromosome haplogroups. Russ J Genet 2004; 40: 326–331.
Khrunin AV, Bebiakova NA, Ivanov VP, Solodilova MA, Limborskaia SA : Polymorphism of Y-chromosomal microsatellites in Russian populations from the northern and southern Russia as exemplified by the populations of Kursk and Arkhangelsk Oblast. Russ J Genet 2005; 41: 922–927.
Das K, Mastana SS : Genetic variation of three VNTR loci in three tribal populations of Orissa, India. Ann Hum Biol 2003; 30: 237–249.
Rosser ZH, Zerjal T, Hurles ME, Adojaan M et al: Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language. Am J Hum Genet 2000; 67: 1526–1543.
Nasidze I, Sarkisian T, Kerimov A, Toneking M : Testing hypotheses of language replacement in the Caucasus: evidence from the Y chromosome. Hum Genet 2003; 112: 255–261.
Nasidze I, Ling EYS, Quinque D et al: Mitochondrial DNA and Y-chromosome variation in the Caucasus. Ann Hum Genet 2004; 68: 205–222.
Al-Zahery N, Semino O, Benuzzi G et al: Y-chromosome and mtDNA polymorphisms in Iraq, a crossroad of the early human dispersal and of post-Neolithic migrations. Mol Phylogenet Evol 2003; 28: 458–472.
Cinnioğlu C, King R, Kivisild R et al: Excavating Y-chromosome haplotype strata in Anatolia. Hum Genet 2004; 114: 127–148.
Regueiro M, Cadenas AM, Gayden T, Underhill PA, Herrera RJ : Iran: tricontinental nexus for Y-chromosome driven migration. Hum Hered 2006; 61: 132–143.
Karafet T, Xu L, Du R et al: Paternal population history of East Asia: sources, patterns, and microevolutionary processes. Am J Hum Genet 2001; 69: 615–628.
Derenko M, Malyarhuk B, Denisova GA et al: Contrasting patterns of Y-chromosome variation in South Siberian populations from Baikal and Altai-Sayan regions. Hum Genet 2006; 118: 591–604.
Antunez-de-Mayolo G, Antunez-de-Mayolo A, Antunez-de-Mayolo P et al: Phylogenetics of Worldwide populations as determined by polymorphic Alu insertions. Electrophoresis 2002; 23: 3346–3356.
Cadenas AM, Zhivotovsky LA, Cavalli-Sforza LL, Underhill PA, Herrera RJ : Y chromosome diversity characterizes the Gulf of Oman. Eur J Hum Genet 2008; 16: 374–386.
Gayden T, Cadenas AM, Regueiro M et al: The Himalayas as a directional barrier to gene flow. Am J Hum Genet 2007; 80: 884–894.
Hammer MF, Horai S : Y chromosomal DNA variation and the peopling of Japan. Am J Hum Genet 1995; 56: 951–962.
Underhill PA, Passarino G, Lin AA et al: The phylogeography of Y chromosome binary haplotypes and the origins of modern human populations. Ann Hum Genet 2001; 65: 43–62.
Kayser M, Krawczak M, Excoffier L et al: An extensive analysis of Y-chromosomal microsatellite haplotypes in globally dispersed human populations. Am J Hum Genet 2001; 68: 990–1018.
Zhivotovsky LA, Underhill PA, Cinnioğlu C et al: The effective mutation rate at Y chromosome short tandem repeats, with application to human population divergence time. Am J Hum Genet 2004; 74: 50–61.
Fenner JN : Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am J Phys Ant 2005; 128: 415–423.
Röhl A : Network 2.0b. A program package for phylogenetic networks. Mathematisches Seminar, Universität Hamburg; Available at http://www.fluxus-engineering.com, 1997.
Luis JR, Rowold DJ, Regueiro M et al: The Levant versus the Horn of Africa: evidence for bidirectional corridors of human migrations. Am J Hum Genet 2004; 74: 532–544.
Rohlf F : NTSYSpc. Setauket, NY: Exter Publishing, 2002.
Guo S, Thompson E : Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 1992; 48: 361–372.
Schneider S, Kueffer JM, Roessli D, Excoffler L : Arlequin v. 2.000: A Software for Population Genetics Data Analysis. Geneva: Genetics and Biometry Laboratory, University of Geneva, 2000.
Fechner A, Quinque D, Rychkov S et al: Boundaries and clines in the West Eurasian Y-chromosome landscape: insights from the European part of Russia. Am J Phys Ant 2008; 137: 41–47.
Kasperaviciute D, Kucinskas V, Stoneking M : Y chromosome and mitochondrial DNA variation in Lithuanians. Ann Hum Genet 2004; 68: 438–452.
Laitinen V, Lahermo P, Sistonen P, Savontaus ML : Y-chromosomal diversity suggests that Baltic males share common Finno-Ugric-speaking forefathers. Hum Hered 2002; 53: 68–78.
Pericic M, Barac L, Klaric IM et al: High-resolution phylogenetic analysis of Southeastern Europe traces major episodes of paternal gene flow among Slavic populations. Mol Biol Evol 2005; 22: 1964–1975.
Nasidze I, Quinque D, Dupanloup I, Cordaux R, Kokshunova L, Stoneking M : Genetic evidence for the Mongolian ancestry of Kalmyks. Am J Phys Anthropol 2005; 128: 846–854.
Bulayeva K, Jorde LB, Ostler C, Watkins S, Bulayev O, Harpending H : Genetics and population history of Caucasus populations. Hum Biol 2003; 75: 837–853.
Gimbutas M : Proto-Indo-European culture: the Kurgan culture during the 5th to the 3rd millennia BC; In Cardona G, Koenigswald HM, Senn A (eds): Indo-European and Indo-Europeans. Philadelphia: University of Pennsylvania Press, 1970, pp 155–198.
Savel’eva EA (ed): Atlas of the Komi Republic. Moscow: Dizain. Moscow: Inter’er Kartographiya, 2001, pp 552.
Kayser M, Brauer S, Cordaux R et al: Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific. Mol Biol Evol 2006; 23: 2234–2244.
Acknowledgements
The work was partially supported by the programs of Presidium of Russian Academy of Sciences: ‘Molecular and Cell Biology’ and ‘Fundamental Sciences for Medicine’ (subprogram ‘Human Polymorphism’), and the Russian Foundation for Basic Research.
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Mirabal, S., Regueiro, M., Cadenas, A. et al. Y-Chromosome distribution within the geo-linguistic landscape of northwestern Russia. Eur J Hum Genet 17, 1260–1273 (2009). https://doi.org/10.1038/ejhg.2009.6
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DOI: https://doi.org/10.1038/ejhg.2009.6


