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Extensive Farming in Estonia Started Through a Sex-Biased bioRxiv preprint doi: https://doi.org/10.1101/112714; this version posted March 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 1 Extensive farming in Estonia started through a sex-biased 2 migration from the Steppe 3 Lehti Saag*1,2, Liivi Varul3, Christiana Lyn Scheib4, Jesper Stenderup5, Morten E. Allentoft5, 4 Lauri Saag2, Luca Pagani2, Maere Reidla1,2, Kristiina Tambets2, Ene Metspalu1,2, Aivar 5 Kriiska6, Eske Willerslev5, Toomas Kivisild1,2,4, Mait Metspalu2 6 1Department of Evolutionary Biology, Institute of Cell and Molecular Biology, University of 7 Tartu; 2Estonian Biocentre; 3School of Humanities, Tallinn University; 4Department of 8 Archaeology and Anthropology, University of Cambridge; 5Centre for GeoGenetics, Natural 9 History Museum of Denmark, University of Copenhagen; 6Department of Archaeology, 10 Institute of History and Archaeology, University of Tartu. 11 Abstract 12 Farming-based economies appear relatively late in Northeast Europe and the extent to which 13 they involve genetic ancestry change is still poorly understood. Here we present the analyses 14 of low coverage whole genome sequence data from five hunter-gatherers and five farmers of 15 Estonia dated to 4,500 to 6,300 years before present. We find evidence of significant differences 16 between the two groups in the composition of autosomal as well as mtDNA, X and Y 17 chromosome ancestries. We find that Estonian hunter-gatherers of Comb Ceramic Culture are 18 closest to Eastern hunter-gatherers. The Estonian first farmers of Corded Ware Culture show 19 high similarity in their autosomes with Steppe Belt Late Neolithic/Bronze Age individuals, 20 Caucasus hunter-gatherers and Iranian farmers while their X chromosomes are most closely 21 related with the European Early Farmers of Anatolian descent. These findings suggest that the 22 shift to intensive cultivation and animal husbandry in Estonia was triggered by the arrival of bioRxiv preprint doi: https://doi.org/10.1101/112714; this version posted March 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 2 23 new people with predominantly Steppe ancestry, but whose ancestors had undergone sex- 24 specific admixture with early farmers with Anatolian ancestry. 25 Introduction 26 The change from hunting and gathering to farming was associated with important demographic 27 and cultural changes in different parts of the world. The process involving changes in life-style 28 and in material culture, such as the introduction of pottery, has often been referred to as the 29 Neolithic transition. This term can become confusing when talking about Eastern and Northern 30 areas of Europe like Estonia where some aspects of the so-called Neolithic package, such as 31 pottery, arrive earlier, whilst the transition from hunting-gathering to farming as the main 32 source of sustenance does not occur until Late Neolithic1. 33 aDNA studies have shown that Mesolithic hunter-gatherer groups of Europe and West Asia 34 were genetically highly differentiated from each other in terms of genetic distances estimated 35 from autosomal loci2–4. At the same time, and likely as a result of multiple population turnovers 36 and bottlenecks5, the Mesolithic hunter-gatherers of Europe displayed a highly uniform pallet 37 of mtDNA with most individuals belonging to haplogroup (hg) U56,7. The early farmers of 38 Europe, who arrived from West Asia more than 8,000 years BP (yr BP)8,9, in contrast belonged 39 to a wide variety of mtDNA haplogroups previously unseen in Europe10,11. These findings have 40 led to the view that the shift to agriculture involved a substantial degree of population 41 replacement and that hunter-gatherers and farmers did not interbreed considerably for the first 42 few thousand years, both in Central Europe12–14 and in Scandinavia15–17. Analyses of autosomal 43 data on a genome-wide scale have revealed that among the present-day populations of Europe, 44 Sardinians show the highest affinity to the early farmers of Europe. The ancient genomes of the 45 earliest farmers from across Europe – including those from Scandinavia15,16, the Alps18, 46 Central2,19,20 and Southern Europe2,21 – cluster closely together and share genetic components bioRxiv preprint doi: https://doi.org/10.1101/112714; this version posted March 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 3 47 with present-day Sardinians and ancient DNA sequences from Anatolian farmers suggesting 48 their common descent from an Anatolian source4,22. It has also been shown that the first farmers 49 of the Fertile Crescent had a clear regional substructure largely copying that of the local hunter- 50 gatherers4. Importantly, the early farmers of Europe derive from Anatolian farmers4,23 and not 51 from the eastern side of the Fertile Crescent3,4. The Yamnaya Culture people from the Steppe 52 region of the Eastern European Plain associated with the next wave of migration into Central 53 Europe2,24,25 on the other hand shared some ancestry with hunter-gatherers of Caucasus and 54 Iran4. 55 The first signs of crop cultivation in Estonia appeared 6,000 yr BP, 2000 years after the first 56 evidence of farming in Southern Europe, while the transition to the intensive cultivation and 57 animal husbandry is estimated to have taken place much later, between 4,800–4,000 yr BP26. 58 This change is associated with a gradual shift from the primarily hunting-gathering-based Comb 59 Ceramic Culture (CCC) to the farming-based Corded Ware Culture (CWC). CCC is thought to 60 have arisen around 5,900 yr BP in areas east of the Baltic Sea and spread as far as Estonia, parts 61 of Finland, Sweden, Russia, Belorussia, and Latvia and Lithuania (Fig 1)27. CCC sites have 62 been found predominantly near bodies of water and it has been suggested that the hunter- 63 gatherer groups, making clay pots that were decorated with a comb-like stamp, largely lived 64 off of fishing, hunting and gathering, as demonstrated by the animal bones found from CCC 65 sites and by stable isotopes (13C and 15N) of human remains27–29. Conversely, the rise of CWC 66 around 4,800 yr BP30 has been associated with the late spread of farming. CWC later reached 67 Finland, Sweden and Norway in the North (Fig 1), Tatarstan in the East, Switzerland and 68 Ukraine in the South, and Belgium and France in the West31–33. Demic diffusion from the 69 Steppe region34 has been recently supported by aDNA evidence and proposed to be associated 70 with the appearance of CWC in Europe2,25. CWC in Estonia is, among other traits, characterized 71 by clay vessels often decorated with cord impressions, boat-shaped stone axes27 and clear bioRxiv preprint doi: https://doi.org/10.1101/112714; this version posted March 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 4 72 evidence of cultivation and animal husbandry, i.e. bones of sheep/goat, pig, and cattle as well 73 as artefacts made of them found mostly from burial sites, numerous occurrences of Cerealia 74 pollen in bog and lake sediments, barley seed and a seed imprint on a pot shard, and stable 75 isotopes (13C and 15N) of human bones35–37. Genetic studies from Central Europe have revealed 76 that CWC burials reflected their familial bonds38 and that these Late Neolithic farmers had 77 already admixed with hunter-gatherers, and also brought novel mtDNA haplogroups to the 78 region12. They were found to be most similar to modern populations from Eastern and Northern 79 Europe, and the Caucasus12,25. Despite its pivotal role in the Yamnaya/CWC expansion, the 80 Eastern European region has been largely overlooked in ancient DNA studies until very 81 recently39. Furthermore, as a consequence, there is very little information about the genetic 82 processes involved in farming reaching this area. Additionally, of all modern European 83 populations analysed so far, East Europeans and particularly Estonians are the ones with the 84 smallest fraction of the Anatolian Neolithic genetic component2, pointing to a potentially 85 different process of farming reaching this area. 86 To shed more light on the genetic changes during the shift to farming based economies in 87 Estonia, we extracted and sequenced aDNA from skeletal remains uncovered in the context of 88 Mesolithic Narva Culture (NC) (7,200–5,900 yr BP), and Neolithic CCC (5,900–3,800 yr BP) 89 and CWC (4,800–4,000 yr BP) from Estonia (Fig 1). We compared these data to sequence and 90 genotype data from modern and ancient populations of Europe, West Asia and Siberia to make 91 inferences about the extent of continuity and genetic change during the end of the Stone Age in 92 Estonia. bioRxiv preprint doi: https://doi.org/10.1101/112714; this version posted March 2, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
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