Ancient DNA from South-East Europe reveals different events during early and middle neolithic influencing the European genetic heritage

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Hervella, Montserrat ^a   Rotea, Mihai ^b   Izagirre, Neskuts ^a   Constantinescu, Mihai ^c   Alonso, Santos ^a   Ioana, Mihai ^d,g   Lazər, Cətəlin ^e   Ridiche, Florin ^f   Soficaru, Andrei Dorian ^c   Netea, Mihai G ^d   De La Rua, Concepcion ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b History Museum of Transylvania   (Romania)

^c ACADEMY OF ROMANIAN SCIENTISTS   (Romania)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e National History Museum of Romania   (Romania)

^f Nature Sciences   (Romania)

^g UNIVERSITY OF MEDICINE AND PHARMACY OF CRAIOVA   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BRONZE AGE; COMPARATIVE STUDY; EUROPEAN; GENETIC ASSOCIATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HAPLOTYPE; HUMAN; INHERITANCE; MOLECULAR PHYLOGENY; NEOLITHIC; POPULATION GENETIC STRUCTURE; POPULATION MIGRATION; ROMANIA; SOUTHERN EUROPEAN; GENETIC VARIATION; GENETICS; GEOGRAPHY; MULTIVARIATE ANALYSIS; POPULATION GENETICS; PRINCIPAL COMPONENT ANALYSIS; TIME FACTOR;

DNA, MITOCHONDRIAL; GENETIC VARIATION; GENETICS, POPULATION; GEOGRAPHY; HAPLOTYPES; HUMANS; MULTIVARIATE ANALYSIS; PRINCIPAL COMPONENT ANALYSIS; ROMANIA; TIME FACTORS;

EID: 84936797749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0128810     Document Type: Article

References (70)

1. Pinhasi R, Thomas MG, Hofreiter MG, Currat M, Burger J (2012) The genetic history of Europeans. Trends Genet 28: 496-505. doi: 10.1016/j.tig.2012.06.006 PMID: 22889475
2. Menozzi P, Piazza A, Cavalli-Sforza LL (1978) Synthetic maps of human gene frequencies in Europeans. Science 201: 786-792. PMID: 356262
3. Cavalli-Sforza LL, Piazza A (1993) Human genomic diversity in Europe: a summary of recent research and prospects for the future. Eur J Hum Genet 1: 3-18. PMID: 7520820
4. Richards MB, Macaulay VA, Bandelt HJ, Sykes BC (1998) Phylogeography of mitochondrial DNA in western Europe. Ann Hum Genet 62: 241-260. PMID: 9803269
5. Richards M, Macaulay VA, Hickey E, Vega E, Sykes B, Guida V, et al. (2000) Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet 67: 1251-1276 PMID: 11032788
6. Currat M, Excoffier L (2005) The effect of the Neolithic expansion on European molecular diversity. Proc Biol Sci 272: 679-688. PMID: 15870030
7. Soares P, Achilli A, Semino O, Davies W, Macaulay V, Bandelt HJ, et al. (2010) The archaeogenetics of Europe. Curr Biol 20: 174-183.
8. Malmström H, Gilbert MT, Thomas MG, Brandstrom M, Stora J, Molnar P, et al. (2009) Ancient DNA reveals lack of continuity between Neolithic hunter-gatherers and contemporary Scandinavians. Curr Biol 19: 1758-62. doi: 10.1016/j.cub.2009.09.017 PMID: 19781941
9. Skoglund P, Malmström H, Raghavan M, Stora J, Hall P, Willerslev E, et al. (2012) Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336: 466-9. doi: 10.1126/science.1216304 PMID: 22539720
10. Skoglund P, Malmström H, Omrak A, Raghavan M, Vadiosera C, Günther T, et al. (2014) Genomic diversity and admixture differs for Stone-Age Scandinavian Foragers and farmers. Science 344: 747-750. doi: 10.1126/science.1253448 PMID: 24762536
11. Bramanti B, Thomas MG, Haak W, Unterlaender M, Jores P, Tambets K, et al. (2009) Genetic discontinuity between local hunter-gatherers and Central Europe's first farmers. Science 326: 137-140. doi: 10.1126/science.1176869 PMID: 19729620
12. Hervella M, Izagirre N, Alonso S, Fregel R, Alonso A, Cabrera VM, 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 PMID: 22563371
13. Sanchez-Quinto F, Schroeder H, Ramirez O, Avila-Arcos MC, Pybus M, Olalde I, et al. (2012) Genomic affinities of two 7,000-year-old Iberian hunter-gatherers. Curr Biol 22: 1494-1499. doi: 10.1016/j.cub.2012.06.005 PMID: 22748318
14. Haak W, Forster P, Bramanti B, Matsumura S, Brandt G, Ta¨nzer M, et al. (2005) Ancient DNA from the first European farmers in 7500-year-old Neolithic sites. Science 310: 1016-1018. PMID: 16284177
15. Haak W, Balanovsky O, Sanchez JJ, Koshel S, Zaporozhchenko V, Adler CJ, 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 PMID: 21085689
16. Deguilloux MF, Soler L, Pemonge MH, Scarre C, Joussaume R, Laporte L (2011) News from the west: ancient DNA from a French megalithic burial chamber. Am J Phys Anthropol 144: 108-118. doi: 10.1002/ajpa.21376 PMID: 20717990
17. Gamba C, Fernandez C, Tirado M, Deguilloux MF, Pemonge MH, Utrilla P, et al. (2012) Ancient DNA from an Early Neolithic Iberian population supports a pioneer colonization by first farmers. Mol Ecol 21: 45-56. doi: 10.1111/j.1365-294X.2011.05361.x PMID: 22117930
18. Guba Hadadi E, Major A, Furka T, Juhasz E, Koós J, et al. (2012) HVS-I polymorphism screening of ancient human mitochondrial DNA provides evidence for N9a discontinuity and East Asian haplogroups in the Neolithic Hungary. J Hum Genet 56: 784-789.
19. Sampietro ML, Lao O, Caramelli DL, Pou R, Marti M, Bertranpetit J, et al. (2007) Palaeogenetic evidence supports a dual model of Neolithic spreading into Europe. Proc R Soc B 274: 2161-2167. PMID: 17609193
20. Lacan M, Keyser C, Ricaut FX, Brucato N, Duranthon F, Guilaine J, et al. (2011) Ancient DNA reveals male diffusion through the Neolithic Mediterranean route. Pro Natl Acad Sci U S A 108: 9788-9791. doi: 10.1073/pnas.1100723108 PMID: 21628562
21. Brandt G, Haak W, Adler CJ, Roth C, Szécsényi-Nagy A, Karimnia S, et al. (2013) Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342: 257-261. doi: 10.1126/science.1241844 PMID: 24115443
22. Fernandez E, Perez-Perez A, Gamba C, Prats E, Cuesta P, Anfruns J, et al. (2014) Ancient DNA Analysis of 8000 B.C Near Eastern Farmers supports an Early Neolithic Pioneer Maritime colonization of Mainland Europe through Cyprus and the Aegean Islans. Plos Genetics 10: e1004401 doi: 10.1371/journal.pgen.1004401 PMID: 24901650
23. Lazaridis L, Patterson N, Mittnik A, Renaud G, MAllick S, Kirsanow K, et al. (2014) Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513: 409-413 doi: 10.1038/nature13673 PMID: 25230663
24. Boric D, Priece TD (2013) Strontium isotopes document greater human mobility at the start of the Balkan Neolithic. Proc Natl Acad Sci U S A 110: 3298-303 doi: 10.1073/pnas.1211474110 PMID: 23401535
25. Pavuk J (1993) Beitrag zur Definition der Protostarecevo-Kultur. Anatolica. 19: 63-74
26. Gronenborn D (2003) Migration, acculturation and culture change in western temperate Eurasia, 6500-5000 cal BC. Documenta Praehistorica 30: 79-91
27. Perles C (2001) The Early Neolithic in Greece: The First Farming Communities in Europe. Cambridge University Press, Cambridge.
28. Ursulescu N, Petrescu-Dâmboviţa M, Monah D (2001) Neo-eneoliticul, in Istoria Românilor I. Bucureşti.
29. Rotea M (2015) Culture, metal and interaction in Transylvanian Prehistory, Cluj-Napoca.
30. Dodd-Opritescu A (1978) Les éléments "steppiques" dans l'énéolithique de Transylvanie. Dacia N S 22: 87-97.
31. Luca SA (1999) Sfârşitul eneoliticului pe teritoriul intracarpatic al României - cultura Bodrogkeresztúr, Alba Iulia.
32. Govedarica B (2004) Zeptertra¨ger - Herrscher der Steppen. Die frühen Ockergra¨ber des a¨lteren Äneolithikums im karpatenbalkanischen Gebiet und im Steppenraum Südost- und Osteuropas. Mainz.
33. Handt O, Krings M, Ward RH, Pa¨a¨bo S (1996) The retrieval of ancient human DNA sequences. Am J Hum Genet 59: 368-376. PMID: 8755923
34. Dumitrescu V (1983) Esquisse d'une préhistoire de la Roumanie jusqu'á la fin de l'âge du bronze, Editura Ştiinţificə şi Enciclopedicə, Bucureşti.
35. Rotea M (2009) Pagini din preistoria Transilvaniei. Epoca bronzului, Cluj-Napoca
36. Hervella M, Izagirre N, Alonso S, Iona M, Netea M, de-la-Rua C (2014) The Carpathian range represents a weak genetic barrier in South-East Europe. BMC Genetics 15: 56. doi: 10.1186/1471-2156-15-56 PMID: 24885208
37. Bailey DW (2000) Balkan Prehistory: Exclusion, Incorporation and Identity. Routledge. London.
38. Bramanti B (2008) Ancient DNA: genetic analysis of aDNA from sixteen skeletons of the Vedrovice collection. Anthropologie XLVI/2-3: 153-160
39. Wilde S, Timpson A, Kirsanow K, Kaiser E, Kaiser M, Unterla¨nder M, et al. (2014) Direct evidence for positive selection of skin, hair and eye pigmentation in Europeans during the last 5000y. Proc Natl Acad Sci U S A 111: 4832-4837. doi: 10.1073/pnas.1316513111 PMID: 24616518
40. Brotherton P, Haak W, Templeton J, Brant G, Soubrier J, Jane Adler C, et al. (2013) Neolithic mitochondrial haplogroup H genomes and the genetic origins of Europeans. Nat Commun 4: e 2656.
41. Haak W, Lazaridis I, Patterson N, Rohland N, Mallick S, Llamas B, et al. (2014) Massive migration from the steppe was a source for Indo-European languages in Europe. Nature (in press) doi: 10.1038/nature14317
42. Bollongino R, Nehlich O, Richards MP, Orschiedt J, Thomas MG, Sell C, et al. (2013) 2000 years of parallel societies in Stone Age Central Europe. Science. 34: 2479-81. PMID: 23947073
43. Ion A, Soficaru AD, Miriţoiu N (2009) Dismembered human remains from the "Neolithic" Cârcea site (Romania). Studii de Preistorie 6: 47-79.
44. Ilie C, Ciobotaru P, Nicu M, Alecsə D, Cotoi OS (2004) Negrileşti, sat Negrileşti, Judeţul Galaţi in Cronica cercetərilor arheologice din România, campania 2003. Institutul Naţional al Patrimoniului. 185. PMID: 21495293
45. Vlassa V (1976) Cea mai veche fazə a complexului cultural Starčevo-Criş în România, Neoliticul Transilvaniei, Cluj Napoca. 198-264.
46. Lazarovici G, Maxim Z (1995) Gura Baciului. Monografie arheologicə, Cluj-Napoca.
47. Lazarovici G, Maxim Z, Meşter M, Bulbuc A, Radu S (1996) Şantierul arheologic Iclod. Campania din 1995. In Acta Musei Napocensis 33: 267-300.
48. Maxim Z (1999) Neo-eneoliticul din Transilvania, Cluj-Napoca.
49. Lazər C (2012) The Catalogue of the Neolithic and Eneolithic Funerary Findings from Romania. Editura Cetatea de Scaun, Târgovite.
50. Luca SA (1999) Sfârşitul eneoliticului pe teritoriul intracarpatic al României - cultura Bodrogkeresztúr. Alba Iulia.
51. Rotea M (2009) Pagini din preistoria Transilvaniei. Epoca bronzului, Cluj-Napoca.
52. Rotea M (2014) Culture, metal and interaction, Cluj-Napoca.
53. Gimbutas M (1997) The Kurgan Culture and the indo-europeanization of Europe. Selected articles from 1952 to 1993. Washington.
54. Heyd V (2011) Yamnaya Groups and Tumuli West of the Black Sea, în Elisabetta Borgna, Silvie Müller Celka (ed.), Ancestral Landscapes: Burial Mounds in the Copper and Bronze Ages. Lyon, 535-555
55. Telegin D, Mallory J (1994) The anthropomorphic stelae of the Ukraine: the early iconography of the Indo-Europeans. Washington.
56. Vulpe M (2001) Petrescu-Dâmboviţa, Epoca bronzului, Istoria Românilor, vol. I: Moştenirea timpurilor îndepərtate, eds Petrescu-Dâmboviţa M, Vulpe A (Editura Enciclopedicə, Bucureşti). 211-294
57. Cooper A, Poinar HN (2000) Ancient DNA: do it right or not at all. Science 289: 1139. PMID: 10970224
58. Hofreiter M, Jaenicke V, Serre D, Haeseler Av A, Pa¨a¨bo S (2001) DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res 29: 4793-4799. PMID: 11726688
59. Pa¨a¨bo S, Pinar H, Serre D, Jaenicke-Despres V, Habler J, Rohland N, et al. (2004).Genetic analyses from ancient DNA. Annu Rev Genet 38: 645-79. PMID: 15568989
60. Gilbert MT, Willerslev E (2006) Authenticity in ancient DNA studies. Medicina Nei Scoli 18: 701-723. PMID: 18175618
61. Ginther C, Issel-Tarver L, King MC (1992) Identifying individuals by sequencing mitochondrial DNA from teeth. Nat Genet 2: 135-138. PMID: 1303263
62. Hagelberg E, Clegg JB (1991) Isolation and characterization of DNA from archaeological bone. Proc Biol Sci 244: 45-50. PMID: 1677195
63. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, Howell N (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23: 147. PMID: 10508508
64. Macaulay V, Richards M, Hickey E, Vega E, Cruciani F, Guida V, et al. (1999) The emerging tree of West Eurasian mtDNAs: a synthesis of control-region sequences and RFLPs. Am J Hum Genet 64;232-49. PMID: 9915963
65. Izagirre N, de la Rúa C (1999) An mtDNA analysis in ancient Basque populations: implications for haplogroup V as a marker for a major paleolithic expansion from southwestern Europe. Am J Hum Genet 65: 199-207. PMID: 10364533
66. Plantinga TS, Alonso S, Izagirre N, Hervella M, Fregel R, van der Meer JW, et al. (2012) Low prevalence of lactase persistence in Neolithic South-West Europe. Eur J Hum Genet 20: 778-782. doi: 10.1038/ejhg.2011.254 PMID: 22234158
67. Nei M (1987) Molecular evolutionary Genetics. New York: Columbia University Press
68. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152: 1079-89. PMID: 10388826
69. Meyer S, Weiss G, von Haeseler A (1999) Pattern of nucleotide substitution and rate heterogeneity in the hypervariable regions I and II of human mtDNA. Genetics, 152:1103-10. PMID: 10388828
70. Santos C, Montiel R, Sierra B, Bettencourt C, Fernandez E, Alvarez L, et al. (2005) Understanding differences between phylogenetic and pedigree-derived mtDNA mutation rate: a model using families from the Azores Islands (Portugal). Mol Biol Evol, 22: 1490-1505. PMID: 15814829