A combined method for DNA analysis and radiocarbon dating from a single sample

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Korlević, Petra ^a   Talamo, Sahra ^a   Meyer, Matthias ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANCIENT DNA;

ANIMAL; ARCHEOLOGY; FOSSIL; HUMAN; PROCEDURES; RADIOMETRIC DATING;

ANIMALS; ARCHAEOLOGY; DNA, ANCIENT; FOSSILS; HUMANS; RADIOMETRIC DATING;

EID: 85048256816     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-22472-w     Document Type: Article

References (62)

1. Ramsey, C. B., Higham, T. & Leach, P. Towards high-precision AMS: Progress and limitations. Radiocarbon 46, 17-24, https://doi.org/10.1017/S0033822200039308 (2004).
2. Van Klinken, G. J. Bone collagen quality indicators for palaeodietary and radiocarbon measurements. J. Archaeol. Sci. 26, 687-695, https://doi.org/10.1006/jasc.1998.0385 (1999).
3. Brock, F., Higham, T., Ditchfield, P. & Ramsey, C. B. Current pretreatment methods for AMS radiocarbon dating at the Oxford Radiocarbon Accelerator Unit (ORAU). Radiocarbon 52, 103-112, https://doi.org/10.1017/S0033822200045069 (2010).
4. Hublin, J. J. et al. Radiocarbon dates from the Grotte du Renne and Saint-Césaire support a Neandertal origin for the Châtelperronian. Proc. Natl. Acad. Sci. USA 109, 18743-18748, https://doi.org/10.1073/pnas.1212924109 (2012).
5. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172, https://doi.org/10.1038/nature14507 (2015).
6. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211, https://doi.org/10.1038/nature14317 (2015).
7. Fu, Q. M. et al. The genetic history of Ice Age Europe. Nature 534, 200-205, https://doi.org/10.1038/nature17993 (2016).
8. Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419-424, https://doi.org/10.1038/nature19310 (2016).
9. Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222-226, https://doi.org/10.1126/science.1224344 (2012).
10. Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43-49, https://doi.org/10.1038/nature12886 (2014).
11. Meyer, M. et al. Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature 531, 504-507, https://doi.org/10.1038/nature17405 (2016).
12. Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053-1060, https://doi.org/10.1038/nature09710 (2010).
13. Sawyer, S. et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals. Proc. Natl. Acad. Sci. USA 112, 15696-15700, https://doi.org/10.1073/pnas.1519905112 (2015).
14. Brown, S. et al. Identification of a new hominin bone from Denisova Cave, Siberia using collagen fingerprinting and mitochondrial DNA analysis. Sci. Rep. 6, 23559, https://doi.org/10.1038/srep23559 (2016).
15. Slon, V. et al. A fourth Denisovan individual. Sci. Adv. 3, e1700186, https://doi.org/10.1126/sciadv.1700186 (2017).
16. Benazzi, S. et al. The makers of the Protoaurignacian and implications for Neandertal extinction. Science 348, 793-796, https://doi.org/10.1126/science.aaa2773 (2015).
17. Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216-219, https://doi.org/10.1038/nature14558 (2015).
18. Hublin, J. J. The modern human colonization of western Eurasia: when and where? Quat. Sci. Rev. 118, 194-210, https://doi.org/10.1016/j.quascirev.2014.08.011 (2015).
19. Taylor, R. E. Radiocarbon dating of bone - to collagen and beyond In Radiocarbon after four decades (eds Taylor, E., Long, A. & Kra, R. S.) 375-402 (Springer, 1992).
20. Longin, R. New method of collagen extraction for radiocarbon dating. Nature 230, 241-242, https://doi.org/10.1038/230241a0 (1971).
21. Talamo, S. & Richards, M. A comparison of bone pretreatment methods for AMS dating of samples >30,000 BP. Radiocarbon 53, 443-449, https://doi.org/10.1017/S0033822200034573 (2011).
22. Krings, M. et al. Neandertal DNA sequences and the origin of modern humans. Cell 90, 19-30, https://doi.org/10.1016/S0092-8674(00)80310-4 (1997).
23. Rohland, N. & Hofreiter, M. Comparison and optimization of ancient DNA extraction. BioTechniques 42, 343-352, https://doi.org/10.2144/000112383 (2007).
24. Campos, P. F. et al. DNA in ancient bone - Where is it located and how should we extract it? Ann. Anat. 194, 7-16, https://doi.org/10.1016/j.aanat.2011.07.003 (2012).
25. Götherström, A., Collins, M. J., Angerbjörn, A. & Lidén, K. Bone preservation and DNA amplification. Archaeometry 44, 395-404, https://doi.org/10.1111/1475-4754.00072 (2002).
26. Brundin, M., Figdor, D., Sundqvist, G. & Sjögren, U. DNA binding to hydroxyapatite: a potential mechanism for preservation of microbial DNA. J. Endod. 39, 211-216, https://doi.org/10.1016/j.joen.2012.09.013 (2013).
27. Olsson, I. U. Further tests of the EDTA treatment of bones. Radiocarbon 42, 49-52, https://doi.org/10.1017/S0033822200053042 (2000).
28. Tuross, N. Comparative decalcification methods, radiocarbon dates, and stable isotopes of the VIRI bones. Radiocarbon 54, 837-844, https://doi.org/10.1017/S0033822200047482 (2012).
29. Bernardi, G. Chromatography of nucleic acids on hydroxyapatite. Nature 206, 779-783, https://doi.org/10.1038/206779a0 (1965).
30. Persson, P. A method to recover DNA from ancient bones. Ancient DNA Newsl. 1, 25-27 (1992).
31. Korlević, P. et al. Reducing microbial and human contamination in DNA extractions from ancient bones and teeth. BioTechniques 59, 87-93, https://doi.org/10.2144/000114320 (2015).
32. DeNiro, M. J. Postmortem preservation and alteration of in vivo bone collagen isotope ratios in relation to palaeodietary reconstruction. Nature 317, 806-809, https://doi.org/10.1038/317806a0 (1985).
33. Scott, E. M., Cook, G. T. & Naysmith, P. Error and uncertainty in radiocarbon measurements. Radiocarbon 49, 427-440, https://doi.org/10.1017/S0033822200042351 (2007).
34. Cersoy, S. et al. Radiocarbon dating minute amounts of bone (3-60 mg) with ECHoMICADAS. Sci. Rep. 7, 7141, https://doi.org/10.1038/s41598-017-07645-3 (2017).
35. Fewlass, H. et al. Size matters: Radiocarbon dates of <200 μg ancient collagen samples with AixMICADAS and its gas ion source. Radiocarbon (advance online). https://doi.org/10.1017/rdc.2017.98 (2017).
36. Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl. Acad. Sci. USA 110, 2223-2227, https://doi.org/10.1073/pnas.1221359110 (2013).
37. Gansauge, M. T. & Meyer, M. Selective enrichment of damaged DNA molecules for ancient genome sequencing. Genome Res. 24, 1543-1549, https://doi.org/10.1101/gr.174201.114 (2014).
38. Meyer, M. et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403-406, https://doi.org/10.1038/nature12788 (2014).
39. Prüfer, K. et al. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655-658, https://doi.org/10.1126/science.aao1887 (2017).
40. El-Daoushy, M. F. A. F., Olsson, I. U. & Oro, F. H. The EDTA and HCl methods of pre-treating bones. Geol. Fören. Stockholm Förh. 100, 213-219, https://doi.org/10.1080/11035897809454461 (1978).
41. Tuross, N., Fogel, M. L. & Hare, P. E. Variability in the preservation of the isotopic composition of collagen from fossil bone. Geochim. Cosmochim. Acta 52, 929-935, https://doi.org/10.1016/0016-7037(88)90364-X (1988).
42. Sealy, J., Johnson, M., Richards, M. & Nehlich, O. Comparison of two methods of extracting bone collagen for stable carbon and nitrogen isotope analysis: comparing whole bone demineralization with gelatinization and ultrafiltration. J. Archaeol. Sci. 47, 64-69, https://doi.org/10.1016/j.jas.2014.04.011 (2014).
43. Römpler, H. et al. Nuclear gene indicates coat-color polymorphism in mammoths. Science 313, 62-62, https://doi.org/10.1126/science.1128994 (2006).
44. Döhle, H. J. Pferde im Graben des schwedischen Feldlagers Latdorf in Archäologie am Kalkteich 22 bei Latdorf: die Chemie stimmt! (ed. Harald, M.) 115-117 (Landesamt für Denkmalpflege und Archäologie Sachsen-Anhalt, 2008).
45. Talamo, S. et al. The radiocarbon approach to Neanderthals in a carnivore den site: A well-defined chronology for Teixoneres Cave (Moia, Barcelona, Spain). Radiocarbon 58, 247-265, https://doi.org/10.1017/Rdc.2015.19 (2016).
46. Devièse, T. et al. Direct dating of Neanderthal remains from the site of Vindija Cave and implications for the Middle to Upper Paleolithic transition. Proc. Natl. Acad. Sci. USA 114, 10606-10611, https://doi.org/10.1073/pnas.1709235114 (2017).
47. Dabney, J. et al. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc. Natl. Acad. Sci. USA 110, 15758-15763, https://doi.org/10.1073/pnas.1314445110 (2013).
48. Gansauge, M. T. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Protoc. 8, 737-748, https://doi.org/10.1038/nprot.2013.038 (2013).
49. Gansauge, M. T. et al. Single-stranded DNA library preparation from highly degraded DNA using T4 DNA ligase. Nucleic Acids Res. 45, e79, https://doi.org/10.1093/nar/gkx033 (2017).
50. Slon, V. et al. Neandertal and Denisovan DNA from Pleistocene sediments. Science 356, 605-608, https://doi.org/10.1126/science. aam9695 (2017).
51. Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3, https://doi.org/10.1093/nar/gkr771 (2012).
52. Dabney, J. & Meyer, M. Length and GC-biases during sequencing library amplification: A comparison of various polymerase-buffer systems with ancient and modern DNA sequencing libraries. BioTechniques 52, 87-94, https://doi.org/10.2144/000113809 (2012).
53. Meyer, M. & Kircher, M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010, pdbprot5448, https://doi.org/10.1101/pdb.prot5448 (2010).
54. Renaud, G., Stenzel, U. & Kelso, J. leeHom: adaptor trimming and merging for Illumina sequencing reads. Nucleic Acids Res. 42, e141, https://doi.org/10.1093/nar/gku699 (2014).
55. Slon, V. et al. Mammalian mitochondrial capture, a tool for rapid screening of DNA preservation in faunal and undiagnostic remains, and its application to Middle Pleistocene specimens from Qesem Cave (Israel). Quat. Int. 398, 210-218, https://doi.org/10.1016/j.quaint.2015.03.039 (2016).
56. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760, https://doi.org/10.1093/bioinformatics/btp324 (2009).
57. Brown, T. A., Nelson, D. E., Vogel, J. S. & Southon, J. R. Improved collagen extraction by modified Longin method. Radiocarbon 30, 171-177, https://doi.org/10.1017/S0033822200044118 (1988).
58. Higham, T. F. G., Jacobi, R. M. & Ramsey, C. B. AMS radiocarbon dating of ancient bone using ultrafiltration. Radiocarbon 48, 179-195, https://doi.org/10.1017/S0033822200066388 (2006).
59. Brock, F., Ramsey, C. B. & Higham, T. Quality assurance of ultrafiltered bone dating. Radiocarbon 49, 187-192, https://doi.org/10.1017/S0033822200042107 (2007).
60. Kromer, B., Lindauer, S., Synal, H.-A. & Wacker, L. MAMS-a new AMS facility at the Curt-Engelhorn-Centre for Achaeometry, Mannheim, Germany. Nucl. Instrum. Methods Phys. Res. B 294, 11-13, https://doi.org/10.1016/j.nimb.2012.01.015 (2013).
61. Ramsey, C. B. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337-360, https://doi.org/10.1017/S0033822200033865 (2009).
62. Reimer, P. J. et al. IntCal13 and Marine13 radiocarbon age calibration curves 0-50,000 years cal BP. Radiocarbon 55, 1869-1887, https://doi.org/10.2458/azu-js-rc.55.16947 (2013).