Abstract
Prehistoric Europe experienced a marked cultural and economic shift around 4000 years ago, when the established Neolithic agriculture-based economy was replaced by herding-pastoralist industry. In recent years new data about the genetic structure of human communities living during this transition period began to emerge. At the same time, the genetic identities of the Eneolithic and Early Bronze Age (EBA) inhabitants from a prehistoric cultural crossroad in western North Pontic steppe region remain understudied. This report presents results of the investigation of maternal genetic lineages of individuals buried in kurgans constructed during the Eneolithic–EBA transition in the western part of the North Pontic Region (NPR). Mitochondrial DNA (mtDNA) lineages from the interments belonging to the Eneolithic as well as the EBA cultures such as Yamna (Pit Grave), Catacomb and Babino (Mnogovalikovaya or KMK) were examined. In the 12 successfully haplotyped specimens, 75% of mtDNA lineages consisted of west Eurasian haplogroup U and its U4 and U5 sublineages. Furthermore, we identified a subgroup of east Eurasian haplogroup C in two representatives of the Yamna culture in one of the studied kurgans. Our results indicate the persistence of Mesolithic hunter–gatherer mtDNA lineages in western NPR through the EBA, as well as suggesting a mtDNA lineage continuum connecting the western NPR inhabitants of the Early Metal Ages to the North Pontic Neolithic population groups.
Access options
Subscribe to Journal
Get full journal access for 1 year
$399.00
only $33.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
from$8.99
All prices are NET prices.


References
- 1
Piazza, A., Rendine, S., Minch, E., Menozzi, P., Mountain, J. & Cavalli-Sforza, L. L. Genetics and the origin of European languages. Proc. Natl Acad. Sci. USA 92, 5836–5840 (1995).
- 2
Gimbutas, M. A. in American School of Prehistoric Research, Bulletin No. 20 (ed. Hencken, H.) (Peabody Museum, Harvard University, Camridge, MA, USA, 1956).
- 3
Rassamakin, Y. Y. in Ancestral Landscapes TMO 58 (ed. Muller-Celka, S.) 293–306 (Maison de l’Orient et la Méditerranée, Lyon, France, 2011).
- 4
Petrenko, V. G. Kurgan epokhi paleometalla na poberezh’e Khadzhubejskogo limana. MASP 11, 303–368 (2010).
- 5
Ivanova, S. V., Petrenko, V. G. & Betchinnikova, N. E. Kurgans of Ancient Herdsmen from the Southern Buh and Dniester interfluve, (KP OGT, Odessa, Ukraine, 2005).
- 6
Nikitin, A. G., Newton, J. R. & Potekhina, I. D. Mitochondrial haplogroup C in ancient mitochondrial DNA from Ukraine extends the presence of East Eurasian genetic lineages in Neolithic Central and Eastern Europe. J. Hum. Genet. 57, 610–612 (2012).
- 7
Santos, C., Montiel, R., Anglés, N., Lima, M., Francalacci, P., Malgosa, A. et al. Determination of human caucasian mitochondrial DNA haplogroups by means of a hierarchical approach. Hum. Biol. 76, 431–453 (2004).
- 8
Cooper, A. & Poinar, H. N. Ancient DNA: do it right or not at all. Science 289, 1139 (2000).
- 9
Excoffier, L. & Lischer, H. E. L. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567 (2010).
- 10
Nei, M. Analysis of gene diversity in subdivided populations. Proc. Natl Acad. Sci. USA 70, 3321–3323 (1973).
- 11
Wright, S. Evolution and the Genetics of Populations Vol. 4. Variability Within and Among Natural Populations, (University of Chicago Press, Chicago, IL, USA, 1978).
- 12
Raymond, M. & Rousset, F. An exact test for population differentiation. Evolution 49, 1280–1283 (1995).
- 13
van Oven, M. & Kayser, M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum. Mutat. 30, E386–E394 (2009).
- 14
Wilde, S., Timpson, A., Kirsanow, K., Kaiser, E., Kayser, M., Unterländer, M. et al. Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5000 y. Proc. Natl Acad. Sci. USA 111, 4832–4837 (2014).
- 15
Allentoft, M. E., Sikiora, M., Sjögren, K.-G., Rasmussen, S., Rasmussen, M., Stenderup, J. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).
- 16
Turkina, I. S. & Kazarnitsky, A. A. in Cultures of the Steppe Zone of Eurasia and their Interaction with Ancient Civilizations (ed. Alyoshkin, V. A.) 87–92 (Russian Academy of Science, Institute for the History of Material Culture, St Petersburg, Russian Federation, 2012).
- 17
Melchior, L., Lynnerup, N., Siegismund, H. R., Kivisild, T. & Dissing, J. Genetic diversity among ancient Nordic populations. PLoS ONE 5, e11898 (2010).
- 18
Keyser, C., Bouakaze, C., Crubézy, E., Nikolaev, V. G., Montagnon, D., Reis, T. et al. Ancient DNA provides new insights into the history of south Siberian Kurgan people. Hum. Genet. 126, 395–410 (2009).
- 19
Chikisheva, T. A., Gubina, M. A., Kulikov, I. V., Karafet, T. M., Voevoda, M. I., Romaschenko, A. G. et al. A paleogenetic study of the prehistoric populations of the Altai. Archaeol. Ethnol. Anthropol. Eurasia 32, 130–142 (2007).
- 20
Shimada, M. K., Kim, C.-G, Takahashi, A., Spitsyn, V. A., Ikeo, K. & Gojobori, T. et al. in DNA Polymorphism Vol. 10 (ed. Ishidu, H.) 151–155 (Toyo Shoten, Tokyo, Japan, 2002).
- 21
Kang, L., Zheng, H.-X., Chen, F., Yan, S., Liu, K., Qin, Z. et al. mtDNA lineage expansions in Sherpa population suggest adaptive evolution in Tibetan Highlands. Mol. Biol. Evol. 30, 2579–2587 (2013).
- 22
Potekhina, I. D. Naselenie Ukrainy v epokhi Neolita i rannego Eneolita po antropologicheskim dannym, (National Academy of Sciences of Ukraine, Kiev, Ukraine, 1999).
- 23
Der Sarkissian, C. Mitochondrial DNA in Ancient Human Populations of Europe (PhD thesis, Univ. Adelaide, (2011).
- 24
Achilli, A., Rengo, C., Battaglia, V., Pala, M., Olivieri, A., Fornarino, S. et al. Saami and Berbers—An unexpected mitochondrial DNA link. Am. J. Hum. Genet. 76, 883–886 (2005).
- 25
Raule, N., Sevini, F., Li, S., Barbieri, A., Tallaro, F., Lomartire, L. 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 13, 401–407 (2014).
- 26
Malyarchuk, B., Derenko, M., Grzybowski, T., Perkova, M., Rogalla, U., Vanecek, T. et al. The peopling of Europe from the mitochondrial haplogroup U5 perspective. PLoS ONE 5, e10285 (2010).
- 27
Bramanti, B., Thomas, M. G., Haak, W., Unterlaender, M., Jores, P., Tambets, K. et al. Genetic discontinuity between local hunter–gatherers and Central Europe’s first farmers. Science 326, 137–140 (2009).
- 28
Cardoso, S., Valverde, L., Alfonso-Sánchez, M. A., Palencia-Madrid, L., Elcoroaristizabal, X., Algorta, J. et al. The expanded mtDNA phylogeny of the Franco-Cantabrian region upholds the pre-Neolithic genetic substrate of Basques. PLoS ONE 8, e67835 (2013).
- 29
Davidovic, S., Malyarchuk, B., Aleksic, J. M., Derenko, M., Topalovic, V., Litvinov, A. et al. Mitochondrial DNA perspective of Serbian genetic diversity. Am. J. Phys. Anthropol. 156, 449–465 (2015).
- 30
Malyarchuk, B., Grzybowski, T., Derenko, M., Perkova, M., Vanecek, T., Lazur, J. et al. Mitochondrial DNA phylogeny in Eastern and Western Slavs. Mol. Biol. Evol. 25, 1651–1658 (2008).
- 31
Derenko, M., Malyarchuk, B., Denisova, G., Perkova, M., Litvinov, A., Grzybowski, T. et al. Western Eurasian ancestry in modern Siberians based on mitogenomic data. BMC Evol. Biol. 14, 217 (2014).
- 32
Szécsényi-Nagy, A., Brandt, G., Haak, W., Keerl, V., Jakucs, J., Möller-Rieker, S. et al. Tracing the genetic origin of Europe’s first farmers reveals insights into their social organization. Proc. Biol. Sci. 282, 20150339 (2015).
- 33
Keller, M., Rott, A., Hoke, N., Schwarzberg, H., Regner-Kamlah, B., Harbeck, M. et al. United in death-related by blood? Genetic and archeometric analyses of skeletal remains from the neolithic earthwork bruchsal-aue. Am. J. Phys. Anthropol. 157, 458–471 (2015).
- 34
Bollongino, R., Nehlich, O., Richards, M. P., Orschiedt, J., Thomas, M. G., Sell, C. et al. 2000 Years of parallel societies in Stone Age Central Europe. Science 342, 479–481 (2013).
- 35
Malmström, H., Linderholm, A., Skoglund, P., Storå, J., Sjödin, P., Gilbert, M. T. et al. Ancient mitochondrial DNA from the northern fringe of the Neolithic farming expansion in Europe sheds light on the dispersion process. Philos. Trans. R. Soc. Lond. Ser. B 370, 20130373 (2015).
- 36
Brandt, G., Szécsényi-Nagy, A., Roth, C., Alt, K. W. & Haak, W. Human paleogenetics of Europe—the known knowns and the known unknowns. J. Hum. Evol. 79, 73–92 (2015).
- 37
Molodin, V. I., Pilipenko, A. S., Romaschenko, A. G., Zhuravlev, A. A., Trapezov, R. O., Chikisheva, T. A. et al in Population Dynamics in Prehistory and Early History (eds Kaiser, E., Burger, J. & Schier, W.) 93–112 (De Gruyter, Berlin, Germany, 2012).
- 38
Haak, W., Lazaridis, I., Patterson, N., Rohland, N., Mallick, S., Llamas, B. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015).
- 39
Mathieson, I., Lazaridis, I., Rohland, N., Mallick, S., Patterson, N., Roodenberg, S. A. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).
- 40
Brandt, G., Haak, W., Adler, C. J., Roth, C., Szécsényi-Nagy, A., Karimnia, S. et al. Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342, 257–261 (2013).
- 41
Patokova, E. F., Petrenko, V. G., Burdo, N. B. & Polischuk, L. Y. Pamyatniki Tripol’skoj kul’tury v Severo-Zapadnom Prichernomorje, (Naukova Dumka, Kiev, Ukraine, 1989).
- 42
Nikitin, A. G., Sokhatsky, M. P., Kovaliukh, M. M. & Videiko, M. Y. Comprehensive site chronology and ancient mitochondrial DNA analysis from Verteba Cave—a Trypillian culture site of Eneolithic Ukraine. Interdiscip. Archaeol. Nat. Sci. Archaeol. 1, 9–18 (2010).
- 43
Pustovalov, S. Z. Analiz radiokarbonnykh dat iz pogrebenij yamnoj i katakombnoj obschnostej, opublikovannykh v Baltic-Pontic Studies, No7 (1999). Vita Antiq. 5–6, 45–59 (2003).
- 44
Mallory, J. P. & Adams, D. Q. Encyclopedia of Indo-European Culture, (Fitzroy Dearborn Publishers, Chicago, IL, USA, 1997).
- 45
Musilová, E., Fernandes, V., Silva, N. M., Soares, P., Alshamali, F., Harich, N. et al. Population history of the Red Sea-genetic exchanges between the Arabian Peninsula and East Africa signaled in the mitochondrial DNA HV1 haplogroup. Am. J. Phys. Anthropol. 145, 592–598 (2011).
- 46
Lazaridis, I., Nadel, D., Rollefson, G., Merrett, D. C., Rohland, N., Mallick, S. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016).
- 47
Müller, J. Megaliths and Funnel Beakers: Societies in Change 4100–2700 BC, (Joh. Enschedé Amsterdam BV, Amsterdam, The Netherlands, 2011).
Acknowledgements
We thank Dr Chris Reed for his kind assistance with anthropological evaluations of specimens D1.11, R3.19a, K1.10 and K2.1. The genetic analysis was funded by GVSU faculty research grants to AGN, as well as the Presidential Graduate Award (to JP) and the Student Summer Scholars (S3) grant (to JB). We also thank Jeremy Newton for his contribution to the analysis of the samples. Special thanks to Jean Manco for maintaining a comprehensive up-to-date online database of ancient mtDNA.
Author information
Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Additional information
Supplementary Information accompanies the paper on Journal of Human Genetics website
Supplementary information
Rights and permissions
About this article
Cite this article
Nikitin, A., Ivanova, S., Kiosak, D. et al. Subdivisions of haplogroups U and C encompass mitochondrial DNA lineages of Eneolithic–Early Bronze Age Kurgan populations of western North Pontic steppe. J Hum Genet 62, 605–613 (2017). https://doi.org/10.1038/jhg.2017.12
Received:
Revised:
Accepted:
Published:
Issue Date:
Further reading
-
Mitochondrial DNA Profiles of Individuals from a 12th Century Necropolis in Feldioara (Transylvania)
Genes (2021)
-
The earliest herders of East Asia: Examining Afanasievo entry to Central Mongolia
Archaeological Research in Asia (2021)
-
Mitochondrial genomes from Bronze Age Poland reveal genetic continuity from the Late Neolithic and additional genetic affinities with the steppe populations
American Journal of Physical Anthropology (2020)
-
On the Issue of the Sarmatian Population Genetic Composition in the Lower Volga Region (Paleogenetic Data)
Vestnik Volgogradskogo gosudarstvennogo universiteta. Serija 4. Istorija. Regionovedenie. Mezhdunarodnye otnoshenija (2020)
-
GIS-based Landform Classification of Eneoli thic Archaeological Sites in the Plateau-plain Transition Zone (NE Romania): Habitation Practices vs. Flood Hazard Perception
Remote Sensing (2019)