Ancient DNA Reveals Prehistoric Gene-Flow from Siberia in the Complex Human Population History of North East Europe

English version České info

North East Europe harbors a high diversity of cultures and languages, suggesting a complex genetic history. Archaeological, anthropological, and genetic research has revealed a series of influences from Western and Eastern Eurasia in the past. While genetic data from modern-day populations is commonly used to make inferences about their origins and past migrations, ancient DNA provides a powerful test of such hypotheses by giving a snapshot of the past genetic diversity. In order to better understand the dynamics that have shaped the gene pool of North East Europeans, we generated and analyzed 34 mitochondrial genotypes from the skeletal remains of three archaeological sites in northwest Russia. These sites were dated to the Mesolithic and the Early Metal Age (7,500 and 3,500 uncalibrated years Before Present). We applied a suite of population genetic analyses (principal component analysis, genetic distance mapping, haplotype sharing analyses) and compared past demographic models through coalescent simulations using Bayesian Serial SimCoal and Approximate Bayesian Computation. Comparisons of genetic data from ancient and modern-day populations revealed significant changes in the mitochondrial makeup of North East Europeans through time. Mesolithic foragers showed high frequencies and diversity of haplogroups U (U2e, U4, U5a), a pattern observed previously in European hunter-gatherers from Iberia to Scandinavia. In contrast, the presence of mitochondrial DNA haplogroups C, D, and Z in Early Metal Age individuals suggested discontinuity with Mesolithic hunter-gatherers and genetic influx from central/eastern Siberia. We identified remarkable genetic dissimilarities between prehistoric and modern-day North East Europeans/Saami, which suggests an important role of post-Mesolithic migrations from Western Europe and subsequent population replacement/extinctions. This work demonstrates how ancient DNA can improve our understanding of human population movements across Eurasia. It contributes to the description of the spatio-temporal distribution of mitochondrial diversity and will be of significance for future reconstructions of the history of Europeans.

Vyšlo v časopise: Ancient DNA Reveals Prehistoric Gene-Flow from Siberia in the Complex Human Population History of North East Europe. PLoS Genet 9(2): e32767. doi:10.1371/journal.pgen.1003296
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003296

Souhrn

Zdroje

1. Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The History and Geography of Human Genes Princeton Univ. Press, Princeton NJ.

2. CannRL, StonekingM, WilsonAC (1987) Mitochondrial DNA and human evolution. Nature 325: 31–36.

3. RichardsM, Côrte-RealH, ForsterP, MacaulayV, Wilkinson-HerbotsH, et al. (1996) Paleolithic and Neolithic lineages in the European mitochondrial gene pool. Am J Hum Genet 59: 185–203.

4. RichardsM, MacaulayV, BandeltH, SykesB (1998) Phylogeography of mitochondrial DNA in Western Europe. Ann Hum Genet 62: 241–260.

5. RichardsM, MacaulayV, HickeyE, VegaE, SykesB, et al. (2000) Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet 67: 1251–1276.

6. AchilliA, RengoC, MagriC, BattagliaV, OlivieriA, et al. (2004) The molecular dissection of mtDNA haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool. Am J Hum Genet 75: 910–918.

7. PereiraL, RichardsM, GoiosA, AlonsoA, AlbarránC, et al. (2005) High-resolution mtDNA evidence for the late-glacial resettlement of Europe from an Iberian refugium. Genome Res 15: 19–24.

8. MalyarchukB, GrzybowskiT, DerenkoM, PerkovaM, VanecekT, et al. (2008) Mitochondrial DNA phylogeny in Eastern and Western Slavs. Mol Biol Evol 25: 1651–1658.

9. PalaM, AchilliA, OlivieriA, Hooshiar KashaniB, PeregoUA, et al. (2009) Mitochondrial haplogroup U5b3: a distant echo of the epipaleolithic in Italy and the legacy of the early Sardinians. Am J Hum Genet 84: 814–821.

10. PalaM, OlivieriA, AchilliA, AccetturoM, MetspaluE, et al. (2012) Mitochondrial DNA signals of late glacial recolonization of Europe from near eastern refugia. Am J Hum Genet 90: 915–24.

11. SoaresP, AchilliA, SeminoO, DaviesW, MacaulayV, et al. (2010) The archaeogenetics of Europe. Curr Biol 20: R174–R183.

12. BramantiB, ThomasM, HaakW, UnterlaenderM, JoresP, et al. (2009) Genetic discontinuity between local hunter-gatherers and central Europe's first farmers. Science 326: 137–140.

13. MalmströmH, GilbertM, ThomasM, BrandströmM, StoråJ, et al. (2009) Ancient DNA reveals lack of continuity between neolithic hunter-gatherers and contemporary Scandinavians. Curr Biol 19: 1758–1762.

14. KrauseJ, BriggsA, KircherM, MaricicT, ZwynsN, et al. (2010) A complete mtDNA genome of an early modern human from Kostenki, Russia. Curr Biol 20: 231–236.

15. SampietroM, LaoO, CaramelliD, LariM, PouR, et al. (2007) Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe. Proc Biol Sci 274: 2161–2167.

16. HaakW, BalanovskyO, SanchezJJ, KoshelS, ZaporozhchenkoV, et al. (2010) Ancient DNA from European early Neolithic farmers reveals their near eastern affinities. PLoS Biol 8: e1000536 doi:10.1371/journal.pbio.1000536

17. LacanM, KeyserC, RicautFX, BrucatoN, DuranthonF, et al. (2011) Ancient DNA reveals male diffusion through the Neolithic Mediterranean route. Proc Natl Acad Sci U S A 108: 9788–9791.

18. LacanM, KeyserC, RicautFX, BrucatoN, TarrúsJ, et al. (2011) Ancient DNA suggests the leading role played by men in the Neolithic dissemination. Proc Natl Acad Sci U S A 108: 18255–9.

19. GambaC, FernándezE, TiradoM, DeguillouxMF, PemongeMH, et al. (2011) Ancient DNA from an Early Neolithic Iberian population supports a pioneer colonization by first farmers. Mol Ecol 21: 45–56.

20. HervellaM, IzagirreN, AlonsoS, FregelR, AlonsoA, et al. (2012) Ancient DNA from Hunter-Gatherer and Farmer Groups from Northern Spain Supports a Random Dispersion Model for the Neolithic Expansion into Europe. PLoS ONE 7: e34417 doi:10.1371/journal.pone.0034417

21. SvendsenJI, AlexandersonH, AstakhovVI, DemidovI, DowdeswellJA, et al. (2004) Late quaternary ice sheet history of Northern Eurasia. Quat Sc Rev 1229–1271.

22. KozlowskiJ, BandiHG (1984) The paleohistory of circumpolar arctic colonization. Arctic 37: 359–372.

23. DolukhanovP (1997) The Pleistocene-Holocene transition in Northern Eurasia: Environmental changes and human adaptations. Quat Internat 181–191.

24. ShumkinV (1990) On the ethnogenesis of the Sami: An archaeological view. Acta Borealia 7: 3–2.

25. PriceTD (1991) The Mesolithic of Northern Europe. Annu Rev Anthropol 20: 211–233.

26. JacobsK (1995) Returning to Oleni' ostrov: Social, Economic, and Skeletal Dimensions of a Boreal Forest Mesolithic Cemetery. J Anthropol Archaeol 14: 359–403.

27. ZvelebilM, DolukhanovP (1991) The transition to farming in Eastern and Northern Europe. J W Prehist 5: 233–278.

28. Forte A, Oram R, Pedersen F (2005) Viking Empires. Cambridge University Press.

29. BalanovskyO, RootsiS, PshenichnovA, KivisildT, ChurnosovM, et al. (2008) Two sources of the Russian patrilineal heritage in their Eurasian context. Am J Hum Genet 82: 236–50.

30. Grousset R (1970) The Empire of the Steppes: History of Central Asia. Rutgers University Press.

31. Sammallahti P (1998) The Saami languages: an introduction. Davvi Girji, Kárásjohka/Karasjoki, Vaasa.

32. TambetsK, RootsiS, KivisildT, HelpH, SerkP, et al. (2004) The Western and Eastern roots of the Saami-the story of genetic “outliers” told by mitochondrial DNA and Y chromosomes. Am J Hum Genet 74: 661–682.

33. GuglielminoCR, PiazzaA, MenozziP, Cavalli-SforzaLL (1990) Uralic genes in Europe. Am J Phys Anthropol 83: 57–68.

34. BeckmanL, SikströmC, MikelsaarAV, KruminaA, AmbrasieneD, et al. (1998) Transferrin variants as markers of migrations and admixture between populations in the Baltic Sea region. Hum Hered 48: 185–191.

35. AndrewsR, KubackaI, ChinneryP, LightowlersR, TurnbullD, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23: 147.

36. SajantilaA, LahermoP, AnttinenT, LukkaM, SistonenP, et al. (1995) Genes and languages in Europe: an analysis of mitochondrial lineages. Genome Res 5: 42–45.

37. PlissL, TambetK, LoogväliEL, ProninaN, LazdinsM, et al. (2006) Mitochondrial DNA portrait of Latvians: towards the understanding of the genetic structure of Baltic-speaking populations. Ann Hum Genet 70: 439–458.

38. IngmanM, GyllenstenU (2007) A recent genetic link between Sami and the Volga-Ural region of Russia. Eur J Hum Genet 15: 115–120.

39. AchilliA, RengoC, BattagliaV, PalaM, OlivieriA, et al. (2005) Saami and Berbers–an unexpected mitochondrial DNA link. Am J Hum Genet 76 (5) 883–6.

40. LappalainenT, LaitinenV, SalmelaE, AndersenP, HuoponenK, et al. (2008) Migration waves to the Baltic Sea region. Ann Hum Genet 72: 337–348.

41. JacobsK (1992) Human population differentiation in the peri-Baltic Mesolithic: the odontometrics of Oleneostrovskii mogilnik (Karelia). Human Evolution 7: 33–48.

42. MoiseyevVG, KhartanovichVI (2012) Early Metal Age Crania from Bolshoy Oleniy Island, Barents Sea. Archaeology, Ethnology and Anthropology of Eurasia 40 (1) 145–154.

43. WallaceDC, BrownMD, LottMT (1999) Mitochondrial DNA variation in human evolution and disease. Gene 238: 211–230.

44. IngmanM, KaessmannH, PääboS, GyllenstenU (2000) Mitochondrial genome variation and the origin of modern humans. Nature 408: 708–713.

45. Maca-MeyerN, GonzálezAM, LarrugaJM, FloresC, CabreraVM (2001) Major genomic mitochondrial lineages delineate early human expansions. BMC Genet 2: 13.

46. HerrnstadtC, ElsonJL, FahyE, PrestonG, TurnbullDM, et al. (2002) Reduced-median-network analysis of complete mitochondrial DNA coding region sequences for the major African, Asian, and European haplogroups. Am J Hum Genet 70: 1152–1171.

47. MishmarD, Ruiz-PesiniE, GolikP, MacaulayV, ClarkAG, et al. (2003) Natural selection shaped regional mtDNA variation in humans. Proc Natl Acad Sci U S A 100: 171–176.

48. KongQP, YaoYG, SunC, Bandelt HJ, ZhuCL, et al. (2003) Phylogeny of East Asian mitochondrial DNA lineages inferred from complete sequences. Am J Hum Genet 73: 671–676.

49. AndersonC, RamakrishnanU, ChanY, HadlyE (2005) Serial SimCoal: a population genetics model for data from multiple populations and points in time. Bioinformatics 21: 1733–1734.

50. BeaumontMA, ZhangW, BaldingDJ (2002) Approximate Bayesian computation in population genetics. Genetics 162: 2025–2035.

51. AkaikeH (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19: 716–723.

52. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: A practical information-theoretic approach, 2nd edition. New York: Springer.

53. PosadaD, BuckleyTR (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. Syst Biol 53: 793–808.

54. DerenkoM, MalyarchukB, GrzybowskiT, DenisovaG, DambuevaI, et al. (2007) Phylogeographic analysis of mitochondrial DNA in northern Asian populations. Am J Hum Genet 81: 1025–41.

55. Keyser-TracquiC, CrubézyE, LudesB (2003) Nuclear and mitochondrial DNA analysis of a 2,000-year-old necropolis in the Egyin Gol Valley of Mongolia. Am J Hum Genet 73: 247–260.

56. KeyserC, BouakazeC, CrubézyE, NikolaevV, MontagnonD, et al. (2009) Ancient DNA provides new insights into the history of south Siberian Kurgan people. Hum Genet 126: 395–410.

57. Sánchez-QuintoF, SchroederH, RamirezO, Avila-ArcosMC, PybusM, et al. (2012) Genomic Affinities of Two 7,000-Year-Old Iberian Hunter-Gatherers. Curr Biol

58. SkoglundP, MalmströmH, RaghavanM, StoråJ, HallP, et al. (2012) Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336 (6080) 466–469.

59. BeharDM, van OvenM, RossetS, MetspaluM, LoogväliEL, et al. (2012) A “Copernican” reassessment of the human mitochondrial DNA tree from its root. Am J Hum Genet 90 (4) 675–84.

60. LoogväliEL, RoostaluU, MalyarchukBA, DerenkoMV, KivisildT, et al. (2004) Disuniting uniformity: a pied cladistic canvas of mtDNA haplogroup H in Eurasia. Mol Biol Evol 21 (11) 2012–21.

61. HartzS, TerbergerT, ZhilinM (2010) New AMS-dates for the Upper Volga Mesolithic and the origin of microblade technology in Europe. Quartär 57: 155–169.

62. ZakhVA, RyaboginaNE, ChlachulaNE (2010) Climate and Environmental Dynamics of the Mid- to Late Holocene Settlement in the Tobol-Ishim Forest-Steppe Region, West Siberia. Quatern Int 220: 95–101.

63. DerenkoM, MalyarchukB, GrzybowskiT, DenisovaG, RogallaU, et al. (2010) Origin and post-glacial dispersal of mitochondrial DNA haplogroups C and D in Northern Asia. PLoS ONE 5: e15214 doi:10.1371/journal.pone.0015214

64. MalyarchukB, DerenkoM, DenisovaG, KravtsovaO (2010) Mitogenomic diversity in Tatars from the Volga-Ural region of Russia. Mol Biol Evol 27: 2220–2226.

65. VelichkoAA, CattoNR, Yu KononovM, MorozovaTD, Yu NovenkoE, et al. (2009) Progressively cooler, drier interglacials in southern Russia through the Quaternary: Evidence from the Sea of Azov region. Quatern Int 198 (1–2) 204–219.

66. VybornovAA (2008) New data on radiocarbon chronology of Neolithic ceramics from the Volga-Kama region. Archaeology, Ethnology and Anthropology of Eurasia 36 (4) 15–24.

67. Gronenborn D (2009) Transregional culture contacts and the neolithization process in Northern Central Europe. In: Jordan P, Zvelebil M, editors. Ceramics before Farming: the Origins and Dispersal of Pottery among Hunter-Gatherers of Northern Eurasia from 16 000 BP. London: University College London Institute of Archaeology Publications, Left Coast Press. pp. 527–550.

68. Hommel P (2009) Hunter Gatherer Pottery: an Emerging 14C Chronology. In: Jordan P, Zvelebil M, editors. Ceramics before Farming: the Origins and Dispersal of Pottery among Hunter-Gatherers of Northern Eurasia from 16 000 BP. London: University College London Institute of Archaeology Publications, Left Coast Press.

69. HuntHV, CampanaMG, LawesMC, ParkYJ, BowerMA, et al. (2011) Genetic diversity and phylogeography of broomcorn millet (Panicum miliaceum L.) across Eurasia. Mol Ecol 20: 4756–4771.

70. FrachettiMD (2011) Migration Concepts in Central Eurasian Archaeology. Annu Rev Anthropol 40 (1) 195–212.

71. KlassenL (2004) Jade und Kupfer. Untersuchungen zum Neolithisierungsprozeß im westlichen Ostseeraum unter besonderer Berücksichtigung der Kulturentwicklung Europas 5500-3500 BC. Jysk Arkæologisk Selskabs

72. Hartz S, Lübke H, Terberger T (2007) From fish and seal to sheep and cattle: new research into the process of neolithization in northern Germany. In: Whittle A, Cummings V, editors. Going Over: the Mesolithic-Neolithic Transition in North-West Europe. London: Proceedings of the British Academy 144. pp. 567–594.

73. Larsson L (2007) Mistrust traditions, consider innovations? The Mesolithic-Neolithic transition in Southern Scandinavia. In: Whittle A, Cummings V, editors. Going Over: the Mesolithic-Neolithic Transition in North-West Europe. London: Proceedings of the British Academy 144. pp. 85–104.

74. Gronenborn D (2011) Early pottery in Afroeurasia - Origins and possible routes of dispersal. In: Hartz S, Lüth F, Terberger T, editors. Early Pottery in the Baltic - Dating, Origin, and social Context, International Workshop at Schleswig from 20th to 21st October 2006. Bericht der Römisch-Germanischen Kommission 89. pp. 59–88.

75. ZvelebilM (2006) Mobility, contact, and exchange in the Baltic Sea basin 6000–2000 BC. J Anthropol Archaeol 25: 178–192.

76. PiezonkaH (2008) Neue AMS-Daten zur frühneolithischen Keramikentwicklung in der nordosteuropäischen Waldzone. Est J Archaeol 12: 67–113.

77. Skandfer M (2009) History as if Neolithisation mattered: the transition to Late Stone Age in northern Fennoscandia. In: Glørstad H, Prescott C, editors. Neolithisation as if History Mattered Process of Neolithisation in North-Western Europe, Neolithisation as if History Mattered. Lindome: Bricoleur Press. pp. 85–104.

78. Matiskainen H (2011) The adoption of pottery in Mesolithic Finland - Sources of impulses, when and why? In: Hartz S, Lüth F, Terberger T, editors. Early Pottery in the Baltic - Dating, Origin, and social Context, International Workshop at Schleswig from 20th to 21st October 2006. Bericht der Römisch-Germanischen Kommission 89. pp. 181–192.

79. MalyarchukB, DerenkoM, GrzybowskiT, PerkovaM, RogallaU, et al. (2010) The peopling of Europe from the mitochondrial haplogroup U5 perspective. PLoS ONE 5: e10285 doi:10.1371/journal.pone.0010285

80. von Cramon-TaubadelN, PinhasiR (2011) Craniometric data support a mosaic model of demic and cultural Neolithic diffusion to outlying regions of Europe. Proc Biol Sci 278: 2874–2880.

81. Gurina NN (1956) Oleneostrovski Mogil'nik. In Materialy i Issledovaniya po Arkheologgi SSSR. Moscow: Nauka, Akademia Nauk SSSR.

82. O'SheaJ, ZvelebilM (1984) Oleneostrovskii Mogilnik: Reconstructing Social and Economic Organisation of Prehistoric Hunter-Fishers in Northern Russia. J Anthropol Archaeol 1: 1–40.

83. Wood R (2006) Chronometric and paleodietary studies at the Mesolithic and Neolithic burial ground of Minino, NW Russia. Dissertation for the MSc in archaeological Science. Oxford University.

84. Oshibkina SV (1999) Tanged Point Industries in the North-West of Russia. In: Kozlowski SK, Gurba J, Zaliznyak LL, editors. Tanged Points Cultures in Europe. Lublin.

85. HaakW, ForsterP, BramantiB, MatsumuraS, BrandtG, et al. (2005) Ancient DNA from the first European farmers in 7500-year-old Neolithic sites. Science 310: 1016–1018.

86. Bandelt HJ (2006) Estimation of Mutation Rates and Coalescence Times: Some Caveats. In: Bandelt HJ, Macaulay V, Richards M. Mitochondrial DNA and the evolution of Homo sapiens. Berlin: Springer-Verlag. pp. 64.

87. PääboS, PoinarH, SerreD, Jaenicke-DespresV, HeblerJ, et al. (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38: 645–679.

88. NoonanJP, HofreiterM, SmithD, PriestJR, RohlandN, et al. (2005) Genomic sequencing of Pleistocene cave bears. Science 309: 597–599.

89. MalmströmH, SvenssonEM, GilbertMT, WillerslevE, GötherströmA, et al. (2007) More on contamination: the use of asymmetric molecular behavior to identify authentic ancient human DNA behavior to identify authentic ancient human DNA. Mol Biol Evol 24: 998–1004.

90. AdlerCJ, HaakW, DonlonD, CooperA (2010) Survival and recovery of DNA from ancient teeth and bones. J Archaeol Sci 38: 956–964.

91. ExcoffierL, LavalG, SchneiderS (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47–50.

92. HoS, EndicottP (2008) The crucial role of calibration in molecular date estimates for the peopling of the Americas. Am J Hum Genet 83: 142–146 author reply 146–147.

93. GhirottoS, MonaS, BenazzoA, PaparazzoF, CaramelliD, et al. (2010) Inferring genealogical processes from patterns of Bronze-Age and modern DNA variation in Sardinia. Mol Biol Evol 27: 875–886.