Skip to main content
Log in

Diversity and Structure of Mitochondrial Gene Pools of Slavs in the Ethnogenetic Aspect

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

Data on the variability of the nucleotide sequences of whole mitochondrial genomes in populations of Russians, Poles, and Serbs, which represent, respectively, the groups of East, West, and South Slavs, are reviewed in comparison with similar data for other European peoples. It was shown that the results of the analysis of the variability of whole mitogenomes make it possible to substantially detail the ideas about the structure and diversity of mitochondrial gene pools obtained earlier with other approaches, e.g., analysis of the distribution of haplotypes of mtDNA major noncoding region or the frequencies of mitochondrial haplogroups. It has been demonstrated that Bayesian analysis of large data sets on the variability of whole mitogenomes in the Slavs enabled the identification of between-regional differences in the dynamics of the effective population size over time for Europe. The use of a phylogeographic analysis of modern and paleogenomic data on the variability of whole mitogenomes makes it possible to define unique phylogenetic mtDNA clusters specific to certain ethnic groups and their communities. Their common genetic origin, which dates back to the Bronze and Iron Ages, is demonstrated on the example of three ethnic groups of Slavs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. Alekseeva, T.I., Etnogenez vostochnykh slavyan po dannym antropologii (Ethnogenesis of Eastern Slavs According to Anthropological Data), Moscow: Mosk. Gos. Univ., 1973.

  2. Alekseeva, T.I. and Alekseev, V.P., Anthropological view on the origin of Slavs, Priroda (Moscow), 1989, no. 1, pp. 60–62.

  3. Allentoft, M.E., Sikora, M., Sjögren, K.G., et al., Population genomics of Bronze Age Eurasia, Nature, 2015, vol. 522, pp. 167–172.

    Article  CAS  PubMed  Google Scholar 

  4. Aris-Brosou, S. and Excoffier, L., The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism, Mol. Biol. Evol., 1996, vol. 13, pp. 494–504.

    Article  CAS  PubMed  Google Scholar 

  5. Balanovsky, O., Rootsi, S., Pshenichnov, A., et al., Two sources of the Russian patrilineal heritage in their Eurasian context, Am. J. Hum. Genet., 2008, vol. 82, pp. 236–250.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Batini, C., Hallast, P., Vågene, Å.J., et al., Population resequencing of European mitochondrial genomes highlights sex-bias in Bronze Age demographic expansions, Sci. Rep., 2017, vol. 7, p. e12086.

    Article  CAS  Google Scholar 

  7. Behar, D.M., van Oven, M., Rosset, S., et al., A “Copernican” reassessment of the human mitochondrial DNA tree from its root, Am. J. Hum. Genet., 2012, vol. 90, pp. 675–684.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Busby, G.B.J., Hellenthal, G., Montinaro, F., et al., The role of recent admixture in forming the contemporary West Eurasian genomic landscape, Curr. Biol., 2015, vol. 25, p. 2878.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Comas, D., Calafell, F., Mateu, E., et al., Geographic variation in human mitochondrial DNA control region sequence: the population history of Turkey and its relationship to the European populations, Mol. Biol. Evol., 1996, vol. 13, pp. 1067–1077.

    Article  CAS  PubMed  Google Scholar 

  10. Costa, M.D., Pereira, J.B., Pala, M., et al., A substantial prehistoric European ancestry amongst Ashkenazi maternal lineages, Nat. Commun., 2013, vol. 4, p. e2543.

    Article  CAS  Google Scholar 

  11. Csáky, V., Gerber, D., Koncz, I., et al., Genetic insights into the social organisation of the Avar period elite in the 7th century AD Carpathian Basin, Sci. Rep., 2020, vol. 10, p. e948.

    Article  CAS  Google Scholar 

  12. Csákyová, V., Szécsényi-Nagy, A., Csősz, A., et al., Maternal genetic composition of a medieval population from a Hungarian-Slavic contact zone in Central Europe, PLoS One, 2016, vol. 11, p. e0151206.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Csősz, A., Szécsényi-Nagy, A., Csákyová, V., et al., Maternal genetic ancestry and legacy of 10th century AD Hungarians, Sci. Rep., 2016, vol. 6, p. e33446.

    Article  CAS  Google Scholar 

  14. Davidović, S., Malyarchuk, B., Aleksić, J., et al., Mitochondrial DNA perspective of Serbian genetic diversity, Am. J. Phys. Anthropol., 2015, vol. 156, pp. 449–465.

    Article  PubMed  Google Scholar 

  15. Davidović, S., Malyarchuk, B., Aleksić, J., et al., Mitochondrial super-haplogroup U diversity in Serbians, Ann. Hum. Biol., 2017, vol. 44, pp. 408–418.

    Article  PubMed  Google Scholar 

  16. Davidović, S., Malyarchuk, B., Grzybowski, T., et al., Complete mitogenome data for the Serbian population: the contribution to high quality forensic databases, Int. J. Legal Med., 2020, vol. 134, pp. 1581-1590.

    Article  PubMed  Google Scholar 

  17. Denaro, M., Blanc, H., Johnson, M.J., et al., Ethnic variation in Hpa I endonuclease cleavage patterns of human mitochondrial DNA, Proc. Natl. Acad. Sci. U.S.A., 1981, vol. 78, pp. 5768–5772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Derenko, M., Malyarchuk, B., Bahmanimehr, A., et al., Complete mitochondrial DNA diversity in Iranians, PLoS One, 2013, vol. 8, p. e80673.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Derenko, M., Denisova, G., Malyarchuk, B., et al., Mitogenomic diversity and differentiation of the Buryats, J. Hum. Genet., 2018, vol. 63, pp. 71–81.

    Article  CAS  PubMed  Google Scholar 

  20. Derenko, M., Denisova, G., Malyarchuk, B., et al., Insights into matrilineal genetic structure, differentiation and ancestry of Armenians based on complete mitogenome data, Mol. Genet. Genomics, 2019, vol. 294, pp. 1547–1559.

    Article  CAS  PubMed  Google Scholar 

  21. Drummond, A.J., Nicholls, G.K., Rodrigo, A.G., and Solomon, W., Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data, Genetics, 2002, vol. 161, pp. 1307–1320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Drummond, A.J., Rambaut, A., Shapiro, B., and Pybus, O.G., Bayesian coalescent inference of past population dynamics from molecular sequences, Mol. Biol. Evol., 2005, vol. 22, pp. 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  23. Egyed, B., Brandstätter, A., Irwin, J.A., et al., Mitochondrial control region sequence variations in the Hungarian population: analysis of population samples from Hungary and from Transylvania (Romania), Forensic Sci. Int. Genet., 2007, vol. 1, pp. 158–162.

    Article  PubMed  Google Scholar 

  24. Fraumene, C., Belle, E.M., Castri, L., et al., High resolution analysis and phylogenetic network construction using complete mtDNA sequences in Sardinian genetic isolates, Mol. Biol. Evol., 2006, vol. 23, pp. 2101–2111.

    Article  CAS  PubMed  Google Scholar 

  25. Grzybowski, T., Malyarchuk, B.A., Derenko, M.V., et al., Complex interactions of the Eastern and Western Slavic populations with other European groups as revealed by mitochondrial DNA analysis, Forensic Sci. Int. Genet., 2007, vol. 1, pp. 141–147.

    Article  PubMed  Google Scholar 

  26. Haak, W., Lazarids, I., Patterson, N., et al., Massive migration from the steppe was a source for Indo-European languages in Europe, Nature, 2015, vol. 522, pp. 207–211.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Hellenthal, G., Busby, G.B.J., Band, G., et al., A genetic atlas of human admixture history, Science, 2014, vol. 343, pp. 747–751.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Hofmanová, Z., Kreutzer, S., Hellenthal, G., et al., Early farmers from across Europe directly descended from Neolithic Aegeans, Proc. Natl. Acad. Sci. U.S.A., 2016, vol. 113, pp. 6886–6891.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Gimbutas, M., The Prehistory of Eastern Europe, Part 1: Mesolithic, Neolithic and Copper Age Cultures in Russia and the Baltic Area, Cambridge: Peabody Mus., 1956.

  30. Järve, M., Saag, L., Scheib, C.L., et al., Shifts in the genetic landscape of the Western Eurasian steppe associated with the beginning and end of the Scythian dominance, Curr. Biol., 2019, vol. 29, pp. 2430–2441.

    Article  PubMed  CAS  Google Scholar 

  31. Johnson, M.J., Wallace, D.C., Ferris, S.D., et al., Radiation of human mitochondria DNA types analyzed by restriction endonuclease cleavage patterns, J. Mol. Evol., 1983, vol. 19, pp. 255–271.

    Article  CAS  PubMed  Google Scholar 

  32. Juras, A., Dabert, M., Kushniarevich, A., et al., Ancient DNA reveals matrilineal continuity in present-day Poland over the last two millennia, PLoS One, 2014, vol. 9, p. e110839.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Just, R.S., Scheible, M.K., Fast, S.A., et al., Full mtGenome reference data: development and characterization of 588 forensic-quality haplotypes representing three U.S. populations, Forensic Sci. Int. Genet., 2015, vol. 14, pp. 141–155.

    Article  CAS  PubMed  Google Scholar 

  34. Karachanak, S., Carossa, V., Nesheva, D., et al., Bulgarians vs the other European populations: a mitochondrial DNA perspective, Int. J. Legal Med., 2012, vol. 126, pp. 497–503.

    Article  PubMed  Google Scholar 

  35. Karmin, M., Saag, L., Vicente, M., et al., A recent bottleneck of Y chromosome diversity coincides with a global change in culture, Genome Res., 2015, vol. 25, pp. 459–466.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Khrunin, A.V., Khokhrin, D.V., Filippova, I.N., et al., A genome-wide analysis of populations from European Russia reveals a new pole of genetic diversity in northern Europe, PLoS One, 2013, vol. 8, p. e58552.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kushniarevich, A., Utevska, O., Chuhryaeva, M., et al., Genetic heritage of the Balto-Slavic speaking populations: a synthesis of autosomal, mitochondrial and Y‑chromosomal data, PLoS One, 2015, vol. 10, p. e0135820.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Ler-Splavinskii, T., Origin of the Slavs, Vopr. Yazykozn., 1960, no. 4, pp. 20–30.

  39. Li, S., Besenbacher, S., Li, Y., et al., Variation and association to diabetes in 2000 full mtDNA sequences mined from an exome study in a Danish population, Eur. J. Hum. Genet., 2014, vol. 22, pp. 1040–1045.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, pp. 1451–1452.

    Article  CAS  PubMed  Google Scholar 

  41. Lippold, S., Xu, H., Ko, A., et al., Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences, Invest. Genet., 2014, vol. 5, p. e13.

    Article  Google Scholar 

  42. Lipson, M., Szécsényi-Nagy, A., Mallick, S., et al., Parallel palaeogenomic transects reveal complex genetic history of early European farmers, Nature, 2017, vol. 551, pp. 368–372.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Malyarchuk, B.A., Differentiation and genetic position of slavs among Eurasian ethnic groups as inferred from variation in mitochondrial DNA, Russ. J. Genet., 2001, vol. 37, no. 12, pp. 1437–1443.

    Article  CAS  Google Scholar 

  44. Malyarchuk, B.A., Sources of the mitochondrial gene pool of Russians by the results of analysis of modern and paleogenomic data, Vavilovsk. Zh. Genet. Sel., 2019, vol. 23, no. 5, pp. 588–593.

    Google Scholar 

  45. Malyarchuk, B.A. and Derenko, M.V., Mitochondrial DNA variability in Russians and Ukrainians: implication to the origin of the Eastern Slavs, Ann. Hum. Genet., 2001, vol. 65, pp. 63–78.

    Article  CAS  PubMed  Google Scholar 

  46. Malyarchuk, B.A., Grzybowski, T., Derenko, M.V., et al., Mitochondrial DNA variability in Bosnians and Slovenians, Ann. Hum. Genet., 2003, vol. 67, pp. 412–425.

    Article  CAS  PubMed  Google Scholar 

  47. Malyarchuk, B., Derenko, M., Grzybowski, T., et al., Differentiation of mitochondrial DNA and Y chromosomes in Russian populations, Hum. Biol., 2004, vol. 76, pp. 877–900.

    Article  PubMed  Google Scholar 

  48. Malyarchuk, B.A., Grzybowski, T., Derenko, M., et al., Mitochondrial DNA phylogeny in Eastern and Western Slavs, Mol. Biol. Evol., 2008, vol. 25, pp. 1651–1658.

    Article  CAS  PubMed  Google Scholar 

  49. Malyarchuk, B., Derenko, M., Denisova, G., and Kravtsova, O., Mitogenomic diversity in Tatars from the Volga-Ural region of Russia, Mol. Biol. Evol., 2010, vol. 27, pp. 2220–2226.

    Article  CAS  PubMed  Google Scholar 

  50. Malyarchuk, B.A., Derenko, M.V., and Litvinov, A.N., The macrohaplogroup U structure in Russians, Russ. J. Genet., 2017a, vol. 53, no. 4, pp. 498–503.

    Article  CAS  Google Scholar 

  51. Malyarchuk, B., Litvinov, A., Derenko, M., et al., Mitogenomic diversity in Russians and Poles, Forensic Sci. Int. Genet., 2017b, vol. 30, pp. 51–56.

    Article  CAS  PubMed  Google Scholar 

  52. Malyarchuk, B., Derenko, M., Denisova, G., et al., Whole mitochondrial genome diversity in two Hungarian populations, Mol. Gen. Genomics, 2018, vol. 293, pp. 1255–1263.

    Article  CAS  Google Scholar 

  53. Malyarchuk, B.A., Litvinov, A.N., and Derenko, M.V., Structure and forming of mitochondrial gene pool of Russian population of Eastern Europe, Russ. J. Genet., 2019, vol. 55, no. 5, pp. 622–629.

    Article  CAS  Google Scholar 

  54. Margaryan, A., Lawson, D., Sikora, M., et al., Population genomics of the Viking world, Nature, 2020, vol. 585, pp. 390–396. https://doi.org/10.1038/s41586-020-2688-8

    Article  CAS  PubMed  Google Scholar 

  55. Mielnik-Sikorska, M., Daca, P., Malyarchuk, B., et al., The history of Slavs inferred from complete mitochondrial genome sequences, PLoS One, 2013, vol. 8, p. e54360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Morozova, I., Evsyukov, A., Kon’kov, A., et al., Russian ethnic history inferred from mitochondrial DNA diversity, Am. J. Phys. Anthropol., 2012, vol. 147, pp. 341–351.

    Article  PubMed  Google Scholar 

  57. Müller, J., Rassmann, K., and Videiko, M., Trypillia Mega-Sites and European Prehistory: 4100-3400 BCE, London: Routledge, 2016.

    Book  Google Scholar 

  58. Neparáczki, E., Juhász, Z., Pamjav, H., et al., Genetic structure of the early Hungarian conquerors inferred from mtDNA haplotypes and Y-chromosome haplogroups in a small cemetery, Mol. Genet. Genomics, 2017, vol. 292, pp. 201–214.

    Article  PubMed  CAS  Google Scholar 

  59. Olivieri, A., Sidore, C., Achilli, A., et al., Mitogenome diversity in Sardinians: a genetic window onto an Island’s past, Mol. Biol. Evol., 2017, vol. 34, pp. 1230–1239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Översti, S., Onkamo, P., Stoljarova, M., et al., Identification and analysis of mtDNA genomes attributed to Finns reveal long-stagnant demographic trends obscured in the total diversity, Sci. Rep., 2017, vol. 7, p. e6193.

    Article  CAS  Google Scholar 

  61. Pankratov, V., Litvinov, S., Kassian, A., et al., East Eurasian ancestry in the middle of Europe: genetic footprints of steppe nomads in the genomes of Belarusian Lipka Tatars, Sci. Rep., 2016, vol. 6, p. e30197.

    Article  CAS  Google Scholar 

  62. Piotrowska-Nowak, A., Elson, J.L., Sobczyk-Kopciol, A., et al., New mtDNA association model, MutPred variant load, suggests individuals with multiple mildly deleterious mtDNA variants are more likely to suffer from atherosclerosis, Front. Genet., 2019a, vol. 9, p. 702.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Piotrowska-Nowak, A., Kosior-Jarecka, E., Schab, A., et al., Investigation of whole mitochondrial genome variation in normal tension glaucoma, Exp. Eye Res., 2019b, vol. 178, pp. 186–197.

    Article  CAS  PubMed  Google Scholar 

  64. Pereira, J.B., Costa, M.D., Vieira, D., et al., Reconciling evidence from ancient and contemporary genomes: a major source for the European Neolithic within Mediterranean Europe, Proc. Biol. Sci., 2017, vol. 284, p. e20161976.

    Google Scholar 

  65. Ralph, P. and Coop, G., The geography of recent genetic ancestry across Europe, PLoS Biol., 2013, vol. 11, p. e1001555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Rascovan, N., Sjögren, K.-G., Kristiansen, K., et al., Emergence and spread of basal lineages of Yersinia pestis during the Neolithic decline, Cell, 2019, vol. 176, pp. 295–305.

    Article  CAS  PubMed  Google Scholar 

  67. Raule, N., Sevini, F., Li, S., et al., The co-occurrence of mtDNA mutations on different oxidative phosphorylation subunits, not detected by haplogroup analysis, affects human longevity and is population specific, Aging Cell, 2014, vol. 13, pp. 401–407.

    Article  CAS  PubMed  Google Scholar 

  68. Ray, N., Currat, M., and Excoffier, L., Intra-deme molecular diversity in spatially expanding populations, Mol. Biol. Evol., 2003, vol. 20, pp. 76–86.

    Article  CAS  PubMed  Google Scholar 

  69. Rebała, K., Mikulich, A.I., Tsybovsky, I.S., et al., Y-STR variation among Slavs: evidence for the Slavic homeland in the middle Dnieper basin, J. Hum. Genet., 2007, vol. 52, pp. 406–414.

    Article  PubMed  Google Scholar 

  70. Rogers, A.R. and Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences, Mol. Biol. Evol., 1992, vol. 9, pp. 552–569.

    CAS  PubMed  Google Scholar 

  71. Sarac, J., Saric, T., Augustin, D.H., et al., Maternal genetic heritage of Southeastern Europe reveals a new Croatian isolate and a novel, local sub-branching in the X2 haplogroup, Ann. Hum. Genet., 2014, vol. 78, pp. 178–194.

    Article  CAS  PubMed  Google Scholar 

  72. Sedov, V.V., Proiskhozhdenie i rannyaya istoriya slavyan (Origin and Early History of the Slavs), Moscow: Nauka, 1979.

  73. Sedov, V.V., Slavyane v rannem srednevekov’e (Slavs in the Early Middle Ages), Moscow: Nauka, 1995.

  74. Sedov, V.V., Ethnogenesis of the early Slavs, Vestn. Ross. Akad. Nauk, 2003, vol. 73, pp. 594–605.

    Google Scholar 

  75. Shennan, S., Downey, S.S., Timpson, A., et al., Regional population collapse followed initial agriculture booms in mid-Holocene Europe, Nat. Commun., 2013, vol. 4, p. e2486.

    Article  CAS  Google Scholar 

  76. Skonieczna, K., Malyarchuk, B., Jawień, A., et al., Mitogenomic differences between the normal and tumor cells of colorectal cancer patients, Hum. Mutat., 2018, vol. 39, pp. 691–701.

    Article  CAS  PubMed  Google Scholar 

  77. Soares, P., Ermini, L., Thomson, N., et al., Correcting for purifying selection: an improved human mitochondrial molecular clock, Am. J. Hum. Genet., 2009, vol. 84, pp. 740–759.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Stoljarova, M., King, J.L., Takahashi, M., et al., Whole mitochondrial genome genetic diversity in an Estonian population sample, Int. J. Leg. Med., 2016, vol. 130, pp. 67–71.

    Article  Google Scholar 

  79. Tajima, F., Statistical method for testing the neutral mutation hypothesis by DNA polymorphism, Genetics, 1989, vol. 123, pp. 585–595.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Tajima, F., Statistical analysis of DNA polymorphism, Jpn. J. Genet., 1993, vol. 68, pp. 567–595.

    Article  CAS  PubMed  Google Scholar 

  81. Tömöry, G., Csányi, B., Bogácsi-Szabó, E., et al., Comparison of maternal lineage and biogeographic analyses of ancient and modern Hungarian populations, Am. J. Phys. Anthropol., 2007, vol. 134, pp. 354–368.

    Article  PubMed  Google Scholar 

  82. Woźniak, M., Malyarchuk, B., Derenko, M., et al., Similarities and distinctions in Y chromosome gene pool of Western Slavs, Am. J. Phys. Anthropol., 2010, vol. 142, pp. 540–548.

    Article  PubMed  Google Scholar 

  83. Zheng, H.-X., Yan, S., Qin, Z.-D., and Jin, L., mtDNA analysis of global populations support that major population expansions began before Neolithic Time, Sci. Rep., 2012, vol. 2, p. e745.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to B. A. Malyarchuk.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of humans or animals. This article does not contain any studies involving animals performed by any of the authors.

Additional information

Translated by A. Kazantseva

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Malyarchuk, B.A., Derenko, M.V. Diversity and Structure of Mitochondrial Gene Pools of Slavs in the Ethnogenetic Aspect. Biol Bull Rev 11, 122–133 (2021). https://doi.org/10.1134/S2079086421020067

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086421020067

Keywords:

Navigation