Two Sources of the Russian Patrilineal Heritage in Their Eurasian Context
2008; Elsevier BV; Volume: 82; Issue: 1 Linguagem: Inglês
10.1016/j.ajhg.2007.09.019
ISSN1537-6605
AutoresOleg Balanovsky, Siiri Rootsi, Andrey Pshenichnov, Toomas Kivisild, Mikhail Churnosov, Irina Evseeva, Elvira Pocheshkhova, Margarita Boldyreva, N. K. Yankovsky, Elena Balanovska, Richard Villems,
Tópico(s)Eurasian Exchange Networks
ResumoProgress in the mapping of population genetic substructure provides a core source of data for the reconstruction of the demographic history of our species and for the discovery of common signals relevant to disease research: These two aspects of enquiry overlap in their empirical data content and are especially informative at continental and subcontinental levels. In the present study of the variation of the Y chromosome pool of ethnic Russians, we show that the patrilineages within the pre-Ivan the Terrible historic borders of Russia have two main distinct sources. One of these antedates the linguistic split between West and East Slavonic-speaking people and is common for the two groups; the other is genetically highlighted by the pre-eminence of haplogroup (hg) N3 and is most parsimoniously explained by extensive assimilation of (or language change in) northeastern indigenous Finno-Ugric tribes. Although hg N3 is common for both East European and Siberian Y chromosomes, other typically Siberian or Mongolian hgs (Q and C) have negligible influence within the studied Russian Y chromosome pool. The distribution of all frequent Y chromosome haplogroups (which account for 95% of the Y chromosomal spectrum in Russians) follows a similar north-south clinal pattern among autosomal markers, apparent from synthetic maps. Multidimensional scaling (MDS) plots comparing intra ethnic and interethnic variation of Y chromosome in Europe show that although well detectable, intraethnic variation signals do not cross interethnic borders, except between Poles, Ukrainians, and central-southern Russians, thereby revealing their overwhelmingly shared patrilineal ancestry. Progress in the mapping of population genetic substructure provides a core source of data for the reconstruction of the demographic history of our species and for the discovery of common signals relevant to disease research: These two aspects of enquiry overlap in their empirical data content and are especially informative at continental and subcontinental levels. In the present study of the variation of the Y chromosome pool of ethnic Russians, we show that the patrilineages within the pre-Ivan the Terrible historic borders of Russia have two main distinct sources. One of these antedates the linguistic split between West and East Slavonic-speaking people and is common for the two groups; the other is genetically highlighted by the pre-eminence of haplogroup (hg) N3 and is most parsimoniously explained by extensive assimilation of (or language change in) northeastern indigenous Finno-Ugric tribes. Although hg N3 is common for both East European and Siberian Y chromosomes, other typically Siberian or Mongolian hgs (Q and C) have negligible influence within the studied Russian Y chromosome pool. The distribution of all frequent Y chromosome haplogroups (which account for 95% of the Y chromosomal spectrum in Russians) follows a similar north-south clinal pattern among autosomal markers, apparent from synthetic maps. Multidimensional scaling (MDS) plots comparing intra ethnic and interethnic variation of Y chromosome in Europe show that although well detectable, intraethnic variation signals do not cross interethnic borders, except between Poles, Ukrainians, and central-southern Russians, thereby revealing their overwhelmingly shared patrilineal ancestry. The haploid Y chromosome is one of the most variable genetic systems in humans, and its phylogeny1Y Chromosome ConsortiumA nomenclature system for the tree of human Y-chromosomal binary haplogroups.Genome Res. 2002; 12: 339-348Crossref PubMed Scopus (657) Google Scholar, 2Jobling M.A. Tyler-Smith C. The human Y chromosome: An evolutionary marker comes of age.Nat. Rev. Genet. 2003; 4: 598-612Crossref PubMed Scopus (661) Google Scholar and phylogeography are increasingly better understood, thereby allowing inferences to be made about its variation in space and time, as well as synthesis of the emerging picture with those arising from matrilineal mtDNA phylogeny and autosomal portion of the human genome.3Underhill P.A. Kivisild T. Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations.Annu. Rev. Genet. 2007; 41: 539-564Crossref PubMed Scopus (286) Google Scholar Yet the genetic sampling of Europe has so far been heavily focused on the western parts of the subcontinent, and often only a few sampling spots for an ethnic group is considered to represent the variation in multimillion population of a large territory. The first broad studies of the variation of the patrilineal genetic system in Europe4Semino O. Passarino G. Oefner P.J. Lin A.A. Arbuzova S. Beckman L.E. De Benedictis G. Francalacci P. Kouvatsi A. Limborska S. et al.The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: A Y chromosome perspective.Science. 2000; 290: 1155-1159Crossref PubMed Scopus (621) Google Scholar, 5Rosser Z.H. Zerjal T. Hurles M.E. Adojaan M. Alavantic D. Amorim A. Amos W. Armenteros M. Arroyo E. Barbujani G. et al.Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language.Am. J. Hum. Genet. 2000; 67: 1526-1543Abstract Full Text Full Text PDF PubMed Scopus (458) Google Scholar immediately revealed its marked phylogeographic differentiation. These two pioneering papers and subsequent studies6Tambets K. Rootsi S. Kivisild T. Help H. Serk P. Loogväli E.-L. Tolk H.-V. Reidla M. Metspalu E. Pliss L. et al.The western and eastern roots of the Saami - the story of genetic “outliers” told by mtDNA and Y-chromosome.Am. J. Hum. Genet. 2004; 74: 661-682Abstract Full Text Full Text PDF PubMed Scopus (152) Google Scholar, 7Rootsi S. Magri C. Kivisild T. Benuzzi G. Help H. Bermisheva M. Kutuev I. Barać L. Peričić M. Balanovsky O. et al.Phylogeography of Y-chromosome haplogroup I reveals distinct domains of prehistoric gene flow in Europe.Am. J. Hum. Genet. 2004; 75: 128-137Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar, 8Semino O. Magri C. Benuzzi G. Lin A.A. Al-Zahery N. Battaglia V. Maccioni L. Triantaphyllidis C. Shen P. Oefner P.J. et al.Origin, diffusion, and differentiation of Y-chromosome haplogroups E and J: Inferences on the neolithization of Europe and later migratory events in the Mediterranean area.Am. J. Hum. Genet. 2004; 74: 1023-1034Abstract Full Text Full Text PDF PubMed Scopus (303) Google Scholar, 9Di Giacomo F. Luca F. Popa L.O. Akar N. Anagnou N. Banyko J. Brdicka R. Barbujani G. Papola F. Ciavarella G. et al.Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe.Hum. Genet. 2004; 115: 357-371Crossref PubMed Scopus (91) Google Scholar, 10Peričić M. Lauc L.B. Klaric I.M. Rootsi S. Janicievic B. Rudan I. Terciz R. Rudan P. High-resolution phylogenetic analysis of southeastern Europe traces major episodes of paternal gene flow among slavic populations.Mol. Biol. Evol. 2005; 10: 1964-1975Crossref Scopus (74) Google Scholar have shown that western Europeans carry predominantly haplogroup R1b, whereas eastern Europeans have high frequency of R1a lineages, that southern Slavs are characterized by high frequency of I1b, whereas Scandinavia is enriched with I1a, and that haplogroups J2 and E3b are confined mainly to southern Europe. In more general terms, it has been concluded that geography, rather than language, explains the observed clinal distribution of NRY variation in Europe.5Rosser Z.H. Zerjal T. Hurles M.E. Adojaan M. Alavantic D. Amorim A. Amos W. Armenteros M. Arroyo E. Barbujani G. et al.Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language.Am. J. Hum. Genet. 2000; 67: 1526-1543Abstract Full Text Full Text PDF PubMed Scopus (458) Google Scholar Ethnicity typically emphasizes linguistic, cultural, and often religious, as well as political, aspects ascribed to human groups11Race E. Genetics Working GroupThe use of racial, ethnic, and ancestral categories in human genetics research.Am. J. Hum. Genet. 2005; 77: 519-532Abstract Full Text Full Text PDF PubMed Scopus (155) Google Scholar and might be differently interpreted in various research fields and scholarly traditions. Here, the term is used in a more stringent meaning, combining linguistic identity with historical background of the population, including its territorial identity and biogeographic ancestry. Studies dedicated to Y chromosomal intraethnic variation in Europe and its neighborhood are so far limited. Kayser et al.12Kayser M. Lao O. Anslinger K. Augustin C. Bargel G. Edelmann J. Elias S. Heinrich M. Henke J. Henke L. et al.Significant genetic differentiation between Poland and Germany follows present-day political borders, as revealed by Y-chromosome analysis.Hum. Genet. 2005; 117: 428-443Crossref PubMed Scopus (90) Google Scholar analyzed Polish and German populations and found that genetic boundaries coincide with the political boundary between Poles and Germans. Cinnioğlu et al.13Cinnioğlu C. King R. Kivisild T. Kalfoğlu E. Atasoy S. Cavalleri G.L. Lillie A.S. Roseman C.C. Lin A.A. Prince K. et al.Excavating Y-chromosome haplotype strata in Anatolia.Hum. Genet. 2004; 114: 127-148Crossref PubMed Scopus (288) Google Scholar studied patterns in the geographic distribution of the Y chromosome haplogroups within Turkey. Malyarchuk et al.14Malyarchuk B. Derenko M. Grzybowski T. Lunkina A. Czarny J. Rychkov S. Morozova I. Denisova G. Miscicka-Sliwka D. Differentiation of mitochondrial DNA and Y chromosomes in Russian populations.Hum. Biol. 2004; 76: 877-900Crossref PubMed Scopus (56) Google Scholar investigated differences among southern and central Russian populations, whereas Karlsson et al.,15Karlsson A.O. Wallerstrom T. Gotherstrom A. Holmlund G. Y-chromosome diversity in Sweden - A long-time perspective.Eur. J. Hum. Genet. 2006; 14: 963-970Crossref PubMed Scopus (50) Google Scholar Luca et al.,16Luca F. Di Giacomo F. Benincasa T. Popa L.O. Banyko J. Kracmarova A. Malaspina P. Novelletto A. Brdicka R. Y-chromosomal variation in the Czech Republic.Am. J. Phys. Anthropol. 2007; 132: 132-139Crossref PubMed Scopus (18) Google Scholar and Kasperaviciute et al.17Kasperaviciute D. Kucinskas V. Stoneking M. Y chromosome and mitochondrial DNA variation in Lithuanians.Ann. Hum. Genet. 2004; 68: 438-452Crossref PubMed Scopus (42) Google Scholar examined variation within Sweden, Czech Republic, and Lithuania, respectively. Unfortunately, some other large subcontinental areas in Europe are not studied yet in respect to intraethnic (defined primarily by language and political-border criteria) variation of their Y chromosome pools. East Europe, in particular its southern steppe belt but also the more northern forest zone, have been, throughout millennia, a crossroad for many populations claiming their origin from a vast area stretching from central Europe to the borders of China. Although much of East Europe was inhabited by anatomically modern humans long before the Last Glacial Maximum approximately 20,000 years ago,18Dolukhanov P.M. “Prehistoric revolutions” and languages in Europe.in: Künnap A. The roots of peoples and languages of Northern Eurasia II and III. University of Tartu, Tartu2000: 71-78Google Scholar, 19Anikovich M.V. Sinitsyn A.A. Hoffecker J.F. Holliday V.T. Popov V.V. Lisitsyn S.N. Forman S.L. Levkovskaya G.M. Pospelova G.A. Kuzmina I.E. et al.Early Upper Paleolithic in Eastern Europe and implications for the dispersal of modern humans.Science. 2007; 315: 223-226Crossref PubMed Scopus (109) Google Scholar and the Neolithic offers increasingly rich archaeological evidence for human habitation, there is no direct evidence for the linguistic affiliation of the first pastoral nomads in the East European steppe belt (possibly Indo-Iranian speakers) or the northern forest zone (possibly ancestors of the Finno-Ugric-speaking people). There is virtually no knowledge about the genetics of these prehistoric populations. However, the evidence from cranial morphology suggests that typically East Eurasian, the so-called “mongoloid type,” started to appear at the borders of Europe only much later, partly because of expansion of the Turkic-speaking people who replaced Indo-Iranians in East Europe at the beginning of the Common Era (CE). Although the exact place of the Slavonic homeland is still debated, it is generally accepted that the southeastward and northeastward expansion of the Slavonic-speaking tribes from Central Europe started in approximately 7th–9th centuries CE. Eastward, this process has probably included extensive, long-lasting processes of assimilation of and admixture with populations living in East Europe—Baltic speakers in the west and Finnic speakers in the central-eastern and northern areas—whereas most of the North Pontic area was presumably inhabited by Indo-Iranian and Turkic-speaking tribes (as well as by other groups, bearing in mind the legacy of Magyars). Here, we focus on the intraethnic variation among Russians, the largest in present-day monoethnic population, living in an area covering more than a third of continental Europe. Russian “ethnicity,” understood as indicated above, was finally formed approximately in the 14th-16th centuries within the central-eastern and northern parts of the eastern Europe, whereas the south and the west of this large area became homelands of linguistically closely related Ukrainians and Belorussians. The Grand Duchy of Moscow included many of the Russian princedoms (Figure 1) and formed a core of the historical Russian area. The genetic sampling in this study is restricted to the Russian subpopulations from the historical Russian area, defined here as the territory before the extensive expansion phase since Ivan the Terrible in the mid-16th century and beyond. Most of the present-day ethnic Russians—approximately 100 millions—live currently in the borders of this historic area according to the 2002 year census, and the present sampling (14 regions, 1228 Y chromosomes) is the first that covers this wide area nearly uniformly. Our Y chromosome phylogenetic analysis is designed for studying intraethnic variation of the paternal lineages among Russians and for revealing their putative admixture with non-Russian populations during the history of the Slavic presence in East Europe. With the help of published data, we briefly discuss the hierarchy of NRY variation more broadly in West Eurasia within and between ethnic boundaries. We collected 1228 DNA samples from 14 regional Russian populations. All sampled individuals identified their four grandparents as ethnic Russians, with their mother tongue being Russian. The rural areas and small towns were chosen for sampling so that the influence of more recent migrations could be minimized. Only individuals with all four grandparents born in the local area were sampled. Sampled persons were unrelated at least up to the third degree of relation (cousins were not sampled, second cousins only when not related by direct paternal or maternal lines). Informed consent was obtained in all cases. All populations were collected under the same sampling strategy described above, with the exception of the Vologda samples collected from the recruits. For each sampled population, latitude and longitude information together with its provincial (“oblast”) and district (“raion”) affiliation is given in Table 1.Table 1Localization of the Studied Russian PopulationsGeographic PositionPopulation NumberPopulation nameNOblast (Province)Raion (District)LongitudeLatitudeResponsible Researcher(s)Northern1Mezen54ArkhangelLeshukonsky (Mezen river)45.7464.9Balanovska, EvseevaNorthern2Pinega114ArkhangelPinezhsky (upper Pinega river)46.5363.45Balanovska, BalanovskyNorthern3Krasnoborsk91ArkhangelKrasnoborsky and Lensky45.9461.56Balanovska, EvseevaNorthern4Vologda121VologdaDifferent districts39.959.23BoldyrevaCentral5Unzha52KostromaManturovsky and Mezhevskoy (Unzha river)44.7758.34Balanovska, BalanovskyCentral6Kashin73TverKashinsky37.6157.36Balanovska, BalanovskyCentral7Porhov57PskovPorhovsky and Dedovichsky29.5657.77Balanovska, BalanovskyCentral8Ostrov75PskovOstrovsky28.3257.35Balanovska, BalanovskyCentral9Roslavl107SmolenskRoslavlsky and Ershichsky32.8753.95Balanovska, BalanovskySouthern10Livni110OrelLivnensky37.5952.4Balanovska, ChurnosovSouthern11Pristen45KurskPristensky36.7151.23Balanovska, ChurnosovSouthern12Repievka96VoronezhRepievsky38.6551.08Balanovska, ChurnosovSouthern13Belgorod143BelgorodYakovlevsky, Prohorovsky and Krasnensky36.4850.78Balanovska, ChurnosovSouthern14Kuban Cossacs90AdygeyMaykopsky40.1744.51Balanovska, Pocheshkova Open table in a new tab Fourteen studied populations cover relatively uniformly the central and southern part of the European Russia and the Russian North. Kuban Cossacs, formed in the 18th century in the North Caucasus, is the only group outside this area. Figure 2 shows locations of the sampled populations and a spatial interpolation confidence zone (this zone is outlined by a gray line on maps in Figure 3, Figure 4). The collected samples were genotyped for 32 informative Y chromosome biallelic markers (see footnote of Table 2 for details).Figure 3Distribution of Y Chromosomal Haplogroups R1a, R1b, N3, and N2 in EuropeShow full captionPanels are described as follows: (A), frequency distribution map of haplogroup R1a; (B), frequency distribution map of haplogroup R1b; (C), frequency distribution map of haplogroup N3; and (D), frequency distribution map of haplogroup N2. The correlogram on each map indicates results of the spatial-autocorrelation analysis of the given haplogroup distribution within the studied Russian area. The Moran's I coefficient was calculated in the PASSAGE program40Rosenberg M.S. Pattern Analysis, Spatial Statistics, and Geographic Exegesis. Version 1.1.in: Department of Biology, Arizona State University. PASSAGE, Tempe, AZ2001Google Scholar with binary weight matrix with five distance classes. Absciss shows the distance (in hundreds of kilometers); the longest-distance classes is wider because of less number of distant populations. Nonsignificant values are shown as empty circles; significant values are shown as black (p > 0.01) and gray (p > 0.05) circles.Maps were created with haplogroup frequency data from this study and literature4Semino O. Passarino G. Oefner P.J. Lin A.A. Arbuzova S. Beckman L.E. De Benedictis G. Francalacci P. Kouvatsi A. Limborska S. et al.The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: A Y chromosome perspective.Science. 2000; 290: 1155-1159Crossref PubMed Scopus (621) Google Scholar, 5Rosser Z.H. Zerjal T. Hurles M.E. Adojaan M. Alavantic D. Amorim A. Amos W. Armenteros M. Arroyo E. Barbujani G. et al.Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language.Am. J. Hum. Genet. 2000; 67: 1526-1543Abstract Full Text Full Text PDF PubMed Scopus (458) Google Scholar, 6Tambets K. Rootsi S. Kivisild T. Help H. Serk P. Loogväli E.-L. Tolk H.-V. Reidla M. Metspalu E. Pliss L. et al.The western and eastern roots of the Saami - the story of genetic “outliers” told by mtDNA and Y-chromosome.Am. J. Hum. Genet. 2004; 74: 661-682Abstract Full Text Full Text PDF PubMed Scopus (152) Google Scholar, 7Rootsi S. Magri C. Kivisild T. Benuzzi G. Help H. Bermisheva M. Kutuev I. Barać L. Peričić M. Balanovsky O. et al.Phylogeography of Y-chromosome haplogroup I reveals distinct domains of prehistoric gene flow in Europe.Am. J. Hum. Genet. 2004; 75: 128-137Abstract Full Text Full Text PDF PubMed Scopus (196) Google Scholar, 9Di Giacomo F. Luca F. Popa L.O. Akar N. Anagnou N. Banyko J. Brdicka R. Barbujani G. Papola F. Ciavarella G. et al.Y chromosomal haplogroup J as a signature of the post-neolithic colonization of Europe.Hum. Genet. 2004; 115: 357-371Crossref PubMed Scopus (91) Google Scholar, 10Peričić M. Lauc L.B. Klaric I.M. Rootsi S. Janicievic B. Rudan I. Terciz R. Rudan P. High-resolution phylogenetic analysis of southeastern Europe traces major episodes of paternal gene flow among slavic populations.Mol. Biol. Evol. 2005; 10: 1964-1975Crossref Scopus (74) Google Scholar, 12Kayser M. Lao O. Anslinger K. Augustin C. Bargel G. Edelmann J. Elias S. Heinrich M. Henke J. Henke L. et al.Significant genetic differentiation between Poland and Germany follows present-day political borders, as revealed by Y-chromosome analysis.Hum. Genet. 2005; 117: 428-443Crossref PubMed Scopus (90) Google Scholar, 13Cinnioğlu C. King R. Kivisild T. Kalfoğlu E. Atasoy S. Cavalleri G.L. Lillie A.S. Roseman C.C. Lin A.A. Prince K. et al.Excavating Y-chromosome haplotype strata in Anatolia.Hum. Genet. 2004; 114: 127-148Crossref PubMed Scopus (288) Google Scholar, 15Karlsson A.O. Wallerstrom T. Gotherstrom A. Holmlund G. Y-chromosome diversity in Sweden - A long-time perspective.Eur. J. Hum. Genet. 2006; 14: 963-970Crossref PubMed Scopus (50) Google Scholar, 16Luca F. Di Giacomo F. Benincasa T. Popa L.O. Banyko J. Kracmarova A. Malaspina P. Novelletto A. Brdicka R. Y-chromosomal variation in the Czech Republic.Am. J. Phys. Anthropol. 2007; 132: 132-139Crossref PubMed Scopus (18) Google Scholar, 17Kasperaviciute D. Kucinskas V. Stoneking M. Y chromosome and mitochondrial DNA variation in Lithuanians.Ann. Hum. Genet. 2004; 68: 438-452Crossref PubMed Scopus (42) Google Scholar, 20Barac L. Pericic M. Klaric I.M. Rootsi S. Janicijevic B. Kivisild T. Parik J. Rudan I. Villems R. Rudan P. Y chromosomal heritage of Croatian population and its island isolates.Eur. J. Hum. Genet. 2003; 11: 535-542Crossref PubMed Scopus (69) Google Scholar, 21Rootsi S. Zhivotovsky L.A. Baldovic M. Kayser M. Kutuev I. Khusnutdinova E.K. Voevoda M.I. Osipova L.P. Stoneking M. Ferak V. et al.A counter-clockwise northern route of the Y-chromosome haplogroup N from Southeast Asia towards Europe.Eur. J. Hum. Genet. 2007; 15: 204-211Crossref PubMed Scopus (114) Google Scholar, 33Wells R.S. Yuldasheva N. Ruzibakiev R. Underhill P.A. Evseeva I. Blue-Smith J. Jin L. Su B. Pitchappan R. Shanmugalakshmi S. et al.The Eurasian heartland: A continental perspective on Y-chromosome diversity.Proc. Natl. Acad. Sci. USA. 2001; 98: 10244-10249Crossref PubMed Scopus (351) Google Scholar, 37Nasidze I. Ling E.Y. Quinque D. Dupanloup I. Cordaux R. Rychkov S. Naumova O. Zhukova O. Sarraf-Zadegan N. Naderi G.A. et al.Mitochondrial DNA and Y-chromosome variation in the caucasus.Ann. Hum. Genet. 2004; 68: 205-221Crossref PubMed Scopus (108) Google Scholar, 39Lappalainen T. Koivumäki S. Salmela E. Huoponen K. Sistonen P. Savontaus M.L. Lahermo P. Regional differences among the Finns: A Y-chromosomal perspective.Gene. 2006; 376: 207-215Crossref PubMed Scopus (56) Google Scholar, 41Behar D.M. Thomas M.G. Skorecki K. Hammer M.F. Bulygina E. Rosengarten D. Jones A.L. Held K. Moses V. Goldstein D. et al.Multiple origins of Ashkenazi Levites: Y chromosome evidence for both Near Eastern and European ancestries.Am. J. Hum. Genet. 2003; 73: 768-779Abstract Full Text Full Text PDF PubMed Scopus (88) Google Scholar, 42Bosch E. Calafell F. González-Neira A. Flaiz C. Mateu E. Scheil H.G. Huckenbeck W. Efremovska L. Mikerezi I. Xirotiris N. et al.Paternal and maternal lineages in the Balkans show a homogeneous landscape over linguistic barriers, except for the isolated Aromuns.Ann. Hum. Genet. 2006; 70: 459-487Crossref PubMed Scopus (91) Google Scholar, 43Brion M. Dupuy B.M. Heinrich M. Hohoff C. Hoste B. Ludes B. Mevag B. Morling N. Niederstätter H. Parson W. et al.A collaborative study of the EDNAP group regarding Y-chromosome binary polymorphism analysis.Forensic Sci. Int. 2005; 153: 103-108Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar, 44Cruciani F. Santolamazza P. Shen P. Macaulay V. Moral P. Olckers A. Modiano D. Holmes S. Destro-Bisol G. Coia V. et al.A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes.Am. J. Hum. Genet. 2002; 70: 1197-1214Abstract Full Text Full Text PDF PubMed Scopus (277) Google Scholar, 45Derenko M. Malyarchuk B. Denisova G.A. Wozniak M. Dambueva I. Dorzhu C. Luzina F. Miscicka-Sliwka D. Zakharov I. Contrasting patterns of Y-chromosome variation in South Siberian populations from Baikal and Altai-Sayan regions.Hum. Genet. 2006; 118: 591-604Crossref PubMed Scopus (56) Google Scholar, 46Di Giacomo F. Luca F. Anagnou N. Ciavarella G. Corbo R.M. Cresta M. Cucci F. Di Stasi L. Agostiano V. Giparaki M. et al.Clinal patterns of human Y chromosomal diversity in continental Italy and Greece are dominated by drift and founder effects.Mol. Phylogenet. Evol. 2003; 28: 387-395Crossref PubMed Scopus (56) Google Scholar, 47Kharkov, V.N. (2005). Structure of Y-chromosomal lineages in Siberian populations. PhD thesis (in Russian). Research Institute of Medical Genetics at the Tomsk Scientific Center, Siberian Division of Russian Academy of Medical Sciences, Tomsk.Google Scholar, 48Laitinen V. Lahermo P. Sistonen P. Savontaus M.L. Y-chromosomal diversity suggests that Baltic males share common Finno-Ugric-speaking forefathers.Hum. Hered. 2002; 53: 68-78Crossref PubMed Scopus (23) Google Scholar, 49Marjanovic D. Fornarino S. Montagna S. Primorac D. Hadziselimovic R. Vidovic S. Pojskic N. Battaglia V. Achilli A. Drobnic K. et al.The peopling of modern Bosnia-Herzegovina: Y-chromosome haplogroups in the three main ethnic groups.Ann. Hum. Genet. 2005; 69: 757-763Crossref PubMed Scopus (67) Google Scholar, 50Nasidze I. Quinque D. Dupanloup I. Rychkov S. Naumova O. Zhukova O. Stoneking M. Genetic evidence concerning the origins of South and North Ossetians.Ann. Hum. Genet. 2004; 68: 588-599Crossref PubMed Scopus (21) Google Scholar, 51Nasidze 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: 846-854Crossref PubMed Scopus (38) Google Scholar, 52Nasidze I. Quinque D. Rahmani M. Alemohamad S.A. Stoneking M. Concomitant replacement of language and mtDNA in South Caspian populations of Iran.Curr. Biol. 2006; 16: 668-673Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar, 53Passarino G. Cavalleri G.L. Lin A.A. Cavalli-Sforza L.L. Børresen-Dale A.L. Underhill P.A. Different genetic components in the Norwegian population revealed by the analysis of mtDNA and Y chromosome polymorphisms.Eur. J. Hum. Genet. 2002; 10: 521-529Crossref PubMed Scopus (50) Google Scholar, 54Regueiro M. Cadenas A.M. Gayden T. Underhill P.A. Herrera R.J. Iran: Tricontinental nexus for Y-chromosome driven migration.Hum. Hered. 2006; 61: 132-143Crossref PubMed Scopus (83) Google Scholar, 55Underhill P.A. Myers N.M. Rootsi S. Chow C.E.T Lin A.A. Otillar R. King R. Zhivotovsky L.A. Balanovsky O. Pshenichnov A. et al.New phylogenetic relationship for Y chromosome haplogroup I: Reapprising its phylogeography and prehistory.in: Rethinking the human revolution: New Behavioural & Biological Perspectives on the Origins and Dispersal of Modern Humans. Cambridge University, McDonald Institute for Arhaeological Research Monographs, 2008Google Scholar in the GGMAG program package as described in 56Balanovskaia E.V. Nurbaev S.D. Rychkov Iu G. Computer technology of the genogeographic study of the gene pool. I. Statistical information from the genogeographic map.Genetika. 1994; 30: 951-965PubMed Google Scholar and 57Balanovskaia E.V. Balanovskiĭ O.P. Spitsyn V.A. Bychkovskaia L.S. Makarov S.V. Paĭ G.V. Rusakov A.E. Subbota D.S. The Russian gene pool. Genogeography of serum genetic markers (HP, GC, PI, TF).Genetika. 2001; 37: 1125-1137PubMed Google Scholar. Because of different phylogenetic resolution levels of data from literature, not all of them were included for creating all eight maps. If source identified R1a1 and R1(xR1a1) haplogroups, they were taken for the mapmaking as R1a and R1b, respectively. Gray lines mark the studied Russian area.Population grouping. Most of populations with sample size less than 40 were omitted or pooled. Data on the same group from the different sources with the sample sizes greater than 40 were pooled when exact localities were not specified in all sources. The map scales are different for frequent (R1a, R1b, and N3, 10% scale step) and less frequent haplogroups (the other five, 5% step); for all maps, the first interval indicates virtual absence (less than 1%). The bar graph above the scale shows the portion of the total area covered by the respective scale interval. Abbreviations in the statistical legend indicate the following: K, number of the studied populations; n, number of samples in K populations; and MIN, MEAN, and MAX, the minimal, mean and maximum frequencies on the map.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Figure 4Distribution of Y Chromosomal Haplogroups I1a, I1b, J2, and E3b in EuropeShow full caption(A) Frequency distribution map of haplogroup I1a.(B) Frequency distribution map of haplogroup I1b.(C) Frequency distribution map of haplogroup E3b.(D) Frequency distribution map of haplogroup J2.View Large Image Figure ViewerDownload Hi-res image Download (PPT)Table 2Frequencies of the Y Chromosomal Haplogroups in Russian PopulationsCE3b1E3b3F∗cParagroup F∗ refers to samples with M89-derived state, ancestral state for M9, M201, M170, and 12f2.G1∗dParagroup G1∗ refers to samples with M285 derived state, ancestral state for P20.G2I∗eParagroup I∗ refers to samples with M170 derived state,
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