A common genetic origin for early farmers from mediterranean cardial and central european LBK cultures

Molecular Biology and Evolution

Volumn 32, Issue 12, 2015, Pages 3132-3142

  Olalde, Iñigo ^a   Schroeder, Hannes ^b,c   Sandoval Velasco, Marcela ^b   Vinner, Lasse ^b   Lobón, Irene ^a   Ramirez, Oscar ^a   Civit, Sergi ^d   Borja, Pablo García ^e   Salazar García, Domingo C ^e,f,g,h   Talamo, Sahra ^h   Fullola, Josep María ^d   Oms, Francesc Xavier ^d   Pedro, Mireia ^d   Martínez, Pablo ^d,i   Sanz, Montserrat ^j   Daura, Joan ^d,j   Zilhão, João ^d,j,k   Marquès Bonet, Tomàs ^a,k   Gilbert, M Thomas P ^b   Lalueza Fox, Carles ^a  

^a CSIC   (Spain)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c LEIDEN UNIVERSITY   (Netherlands)

^d UNIVERSITY OF BARCELONA   (Spain)

^e UNIVERSITY OF VALENCIA   (Spain)

^f UNIVERSITY OF CAPE TOWN   (South Africa)

^g AIX MARSEILLE UNIVERSITÉ   (France)

^h MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

ⁱ Universitat de Barcelona ^*  (Spain)

^j UNIVERSITY OF LISBON   (Portugal)

^k INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

more..

Author keywords

Cardial ware; Migration; Neolithic; Paleogenomics

Indexed keywords

AGRICULTURAL WORKER; ANTIQUITY; ARTICLE; BALKAN PENINSULA; CENTRAL EUROPEAN; CULTURAL ANTHROPOLOGY; FEMALE; GENE SEQUENCE; HUMAN; HUMAN GENOME; MAJOR CLINICAL STUDY; MALE; MIGRATION; PORTUGAL; SOUTHERN EUROPE; SPAIN; AGRICULTURE; CAUCASIAN; DNA SEQUENCE; ETHNIC GROUP; GENETIC VARIATION; GENETICS; HAPLOTYPE; ITALY; NUCLEOTIDE SEQUENCE; POPULATION GENETICS;

MITOCHONDRIAL DNA;

AGRICULTURE; BASE SEQUENCE; CULTURE; DNA, MITOCHONDRIAL; EMIGRATION AND IMMIGRATION; ETHNIC GROUPS; EUROPEAN CONTINENTAL ANCESTRY GROUP; FARMERS; GENETIC VARIATION; GENETICS, POPULATION; GENOME, HUMAN; HAPLOTYPES; HUMANS; ITALY; MEDITERRANEAN REGION; SEQUENCE ANALYSIS, DNA; SPAIN;

EID: 84948176458     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msv181     Document Type: Article

References (62)

1. 1000 Genomes Project Consortium. 2012. An integrated map of genetic variation from 1,092 human genomes. Nature 491:56-65.
2. Adler CJ, Haak W, Donlon D, Cooper A. 2011. Survival and recovery of DNA from ancient teeth and bones. J Archaeol Sci. 38:956-964.
3. Alexander DH, Novembre J, Lange K. 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19:1655-1664.
4. Allentoft ME, Sikora M, Sjögren K-G, Rasmussen S, Rasmussen M, Stenderup J, Damgaard PB, Schroeder H, Ahlström T, Vinner L, et al. 2015. Population genomics of Bronze Age Eurasia. Nature 522:167-172.
5. 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.
6. Ávila-Arcos MC, Sandoval-Velasco M, Schroeder H, Carpenter ML, Malaspinas A-S, Wales N, Peñaloza F, Bustamante CD, Gilbert MTP. 2015. Comparative performance of two whole-genome capture methodologies on ancient DNA Illumina libraries. Methods Ecol Evol. 6:725-734.
7. Beleza S, Santos AM, McEvoy B, Alves I, Martinho C, Cameron E, Shriver MD, Parra EJ, Rocha J. 2013. The timing of pigmentation lightening in Europeans. Mol Biol Evol. 30:24-35.
8. Brandt G, Haak W, Adler CJ, Roth C, Szécsényi-Nagy A, Karimnia S, Möller-Rieker S, Meller H, Ganslmeier R, Friederich S, et al. 2013. Ancient DNA reveals key stages in the formation of central European mitochondrial genetic diversity. Science 342:257-261.
9. Briggs AW, Stenzel U, Johnson PLF, Green RE, Kelso J, Prüfer K, Meyer M, Krause J, Ronan MT, Lachmann M, et al. 2007. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci U S A. 104:14616-14621.
10. Brotherton P, Endicott P, Sanchez JJ, Beaumont M, Barnett R, Austin J, Cooper A. 2007. Novel high-resolution characterization of ancient DNA reveals C > U-type base modification events as the sole cause of post mortem miscoding lesions. Nucleic Acids Res. 35:5717-5728.
11. Busing FMTA, Meijer E, Van Der Leeden R. 1999. Delete-m Jackknife for Unequal m. Stat Comput. 9:3-8.
12. Cardoso S, Valverde L, Alfonso-Sánchez MA, Palencia-Madrid L, Elcoroaristizabal X, Algorta J, Catarino S, Arteta D, Herrera RJ, Zarrabeitia MT, et al. 2013. The expanded mtDNA phylogeny of the Franco-Cantabrian region upholds the pre-neolithic genetic substrate of Basques. PLoS One 8:e67835.
13. Carpenter ML, Buenrostro JD, Valdiosera C, Schroeder H, Allentoft ME, Sikora M, Rasmussen M, Gravel S, Guillén S, Nekhrizov G, et al. 2013. Pulling out the 1%: Whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am J Hum Genet. 93:852-864.
14. Cavalli-Sforza LL, Menozzi P, Piazza A. 1994. The history and geography of human genes. Princeton (NJ): Princeton University Press.
15. Damgaard PB, Margaryan A, Schroeder H, Orlando L, Willerslev E, Allentoft ME. 2015. Improving access to endogenous DNA in ancient bones and teeth. Sci Rep. 5:11184.
16. Deguilloux M-F, Soler L, Pemonge M-H, 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.
17. Der Sarkissian C, Ermini L, Jónsson H, Alekseev AN, Crubezy E, Shapiro B, Orlando L. 2014. Shotgun microbial profiling of fossil remains. Mol Ecol. 23:1780-1798.
18. Durand EY, Patterson N, Reich D, Slatkin M. 2011. Testing for ancient admixture between closely related populations. Mol Biol Evol. 28:2239-2252.
19. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM, Bondarev AA, Johnson PLF, Aximu-Petri A, Prüfer K, de Filippo C, et al. 2014. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514:445-449.
20. Fu Q, Mittnik A, Johnson PLF, Bos K, Lari M, Bollongino R, Sun C, Giemsch L, Schmitz R, Burger J, et al. 2013. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr Biol. 23:553-559.
21. Gamba C, Fernández E, Tirado M, Deguilloux MF, Pemonge MH, Utrilla P, Edo M, Molist M, Rasteiro R, Chikhi L, et al. 2012. Ancient DNA from an Early Neolithic Iberian population supports a pioneer colonization by first farmers. Mol Ecol. 21:45-56.
22. Gamba C, Jones ER, Teasdale MD, McLaughlin RL, Gonzalez-Fortes G, Mattiangeli V, Domboróczki L, Kovári I, Pap I, Anders A, et al. 2014. Genome flux and stasis in a five millennium transect of European prehistory. Nat Commun. 5:5257.
23. García-Garcerà M, Gigli E, Sanchez-Quinto F, Ramirez O, Calafell F, Civit S, Lalueza-Fox C. 2011. Fragmentation of contaminant and endogenous DNA in ancient samples determined by shotgun sequencing; prospects for human palaeogenomics. PLoS One 6:e24161.
24. Grossman SR, Andersen KG, Shlyakhter I, Tabrizi S, Winnicki S, Yen A, Park DJ, Griesemer D, Karlsson EK, Wong SH, et al. 2013. Identifying recent adaptations in large-scale genomic data. Cell 152:703-713.
25. Haak W, Lazaridis I, Patterson N, Rohland N, Mallick S, Llamas B, Brandt G, Nordenfelt S, Harney E, Stewardson K, et al. 2015. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522:207-211.
26. Hofreiter M, Paijmans JLA, Goodchild H, Speller CF, Barlow A, Fortes GG, Thomas JA, Ludwig A, Collins MJ. 2014. The future of ancient DNA: technical advances and conceptual shifts. Bioessays 37:284-293.
27. Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG. 2009. The origins of lactase persistence in Europe. PLoS Comput Biol. 5:e1000491.
28. Jónsson H, Ginolhac A, Schubert M, Johnson PLF, Orlando L. 2013. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29:1682-1684.
29. Keller A, Graefen A, Ball M, Matzas M, Boisguerin V, Maixner F, Leidinger P, Backes C, Khairat R, Forster M, et al. 2012. New insights into the Tyrolean Iceman's origin and phenotype as inferred by wholegenome sequencing. Nat Commun. 3:698.
30. Kloss-Brandstätter A, Pacher D, Schönherr S, Weissensteiner H, Binna R, Specht G, Kronenberg F. 2011. Haplo Grep: a fast and reliable algorithm for automatic classification of mitochondrial DNA haplogroups. Hum Mutat. 32:25-32.
31. Laayouni H, Calafell F, Bertranpetit J. 2010. A genome-wide survey does not show the genetic distinctiveness of Basques. Hum Genet. 127:455-458.
32. Lacan M, Keyser C, Ricaut F-X, Brucato N, Duranthon F, Guilaine J. 2011. Ancient DNA reveals male diffusion through the Neolithic Mediterranean route. Proc Natl Acad Sci U S A. 108:9788-9791.
33. Lacan M, Keyser C, Ricaut F-X, Brucato N, Tarrús J, Bosch A, Guilaine J, Crubézy E, Ludes B. 2011. Ancient DNA suggests the leading role played by men in the Neolithic dissemination. Proc Natl Acad Sci U S A. 108:18255-18259.
34. Lazaridis I, Patterson N, Mittnik A, Renaud G, Mallick S, Kirsanow K, Sudmant PH, Schraiber JG, Castellano S, Lipson M, et al. 2014. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513:409-413.
35. Lee EJ, Makarewicz C, Renneberg R, Harder M, Krause-Kyora B, Müller S, Ostritz S, Fehren-Schmitz L, Schreiber S, Müller J, et al. 2012. Emerging genetic patterns of the european neolithic: perspectives from a late neolithic bell beaker burial site in Germany. Am J Phys Anthropol. 148:571-579.
36. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
37. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25:2078-2079.
38. Lindgreen S. 2012. Adapter Removal: easy cleaning of next-generation sequencing reads. BMC Res Notes. 5:337.
39. Martins H, Oms FX, Pereira L, Pike AWG, Rowsell K, Zilhão J. 2015. Radiocarbon dating the beginning of the Neolithic in Iberia: new results, new problems. J Mediterr Archaeol. 28:105-131.
40. McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. 2010. The Genome Analysis Toolkit: a Map Reduce framework for analyzing nextgeneration DNA sequencing data. Genome Res. 20:1297-1303.
41. Meyer M, Kircher M. 2010. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. Available from: http://dx.doi.org/10.1101/prot5448
42. Olalde I, Allentoft ME, Sánchez-Quinto F, Santpere G, Chiang CWK, DeGiorgio M, Prado-Martinez J, Rodríguez JA, Rasmussen S, Quilez J, et al. 2014. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507:225-228.
43. Olalde I, Lalueza-Fox C. 2015. Modern humans' paleogenomics and the new evidences on the European prehistory. Sci Technol Archaeol Res. 1:STAR20151120548.
44. Orlando L, Ginolhac A, Raghavan M, Vilstrup J, Rasmussen M, Magnussen K, Steinmann KE, Kapranov P, Thompson JF, Zazula G, et al. 2011. True single-molecule DNA sequencing of a pleistocene horse bone. Genome Res. 21:1705-1719.
45. Patterson N, Price AL, Reich D. 2006. Population structure and eigenanalysis. PLoS Genet. 2:e190.
46. Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8:e1002967.
47. Purcell S, Neale B, Todd-brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, Bakker PIW De, Daly MJ, et al. 2007. PLINK : a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81:559-575.
48. Raghavan M, Skoglund P, Graf KE, Metspalu M, Albrechtsen A, Moltke I, Rasmussen S, Stafford TW, Orlando L, Metspalu E, et al. 2014. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505:87-91.
49. Reich D, Thangaraj K, Patterson N, Price AL, Singh L. 2009. Reconstructing Indian population history. Nature 461:489-494.
50. Renfrew C, Bahn P. 1991. Archaeology theories, methods, and practice. New York: Thames and Hudson.
51. Rohland N, Hofreiter M. 2007. Ancient DNA extraction from bones and teeth. Nat Protoc. 2:1756-1762.
52. Sánchez-Quinto F, Schroeder H, Ramirez O, Avila-Arcos MC, Pybus M, Olalde I, Velazquez AMV, Marcos MEP, Encinas JMV, Bertranpetit J, et al. 2012. Genomic affinities of two 7,000-year-old Iberian huntergatherers. Curr Biol. 22:1494-1499.
53. Schroeder H, Ávila-Arcos MC, Malaspinas A-S, Poznik GD, Sandoval-Velasco M, Carpenter ML, Moreno-Mayar JV, Sikora M, Johnson PLF, Allentoft ME, et al. 2015. Genome-wide ancestry of 17th-century enslaved Africans from the Caribbean. Proc Natl Acad Sci U S A. 112:3669-3673.
54. Seguin-Orlando A, Korneliussen TS, Sikora M, Malaspinas A, Manica A, Moltke I, Westaway M, Lambert D, Khartanovich V, Wall JD, et al. 2014. Genomic structure in Europeans dating back at least 36,200 years. Science 346:1113-1118.
55. Skoglund P, Malmström H, Omrak A, Raghavan M, Valdiosera C, Günther T, Hall P, Tambets K, Parik J, Karl-Göran S, et al. 2014. Genomic diversity and admixture differs for stone-age Scandinavian foragers and farmers. Science 201:786-792.
56. Skoglund P, Malmström H, Raghavan M, Storå J, Hall P, Willerslev E, Gilbert MTP, Götherström A, Jakobsson M. 2012. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336:466-469.
57. Skoglund P, Storå J, Götherström A, Jakobsson M. 2013. Accurate sex identification of ancient human remains using DNA shotgun sequencing. J Archaeol Sci. 40:4477-4482.
58. Walsh S, Chaitanya L, Clarisse L, Wirken L, Draus-Barini J, Kovatsi L, Maeda H, Ishikawa T, Sijen T, de Knijff P, et al. 2014. Developmental validation of the HIrisPlex system: DNA-based eye and hair colour prediction for forensic and anthropological usage. Forensic Sci Int Genet. 9:150-161.
59. Walsh S, Liu F, Wollstein A, Kovatsi L, Ralf A, Kosiniak-Kamysz A, Branicki W, Kayser M. 2013. The HIrisPlex system for simultaneous prediction of hair and eye colour from DNA. Forensic Sci Int Genet. 7:98-115.
60. Whittle A. 1996. Europe in the Neolithic: the creation of new worlds. Cambridge: Cambridge University Press.
61. Zilhão J. 1993. The spread of agro-pastoral economies across Mediterranean Europe: a view from the far west. J Mediterr Archaeol. 6:5-63.
62. Zilhão J. 2001. Radiocarbon evidence for maritime pioneer colonization at the origins of farming in west Mediterranean Europe. Proc Natl Acad Sci U S A. 98:14180-14185.