From the field to the laboratory: Controlling DNA contamination in human ancient DNA research in the high-throughput sequencing era

Science and Technology of Archaeological Research

Volumn 3, Issue 1, 2017, Pages 1-14

  Llamas, Bastien ^a   Valverde, Guido ^a   Fehren Schmitz, Lars ^b   Weyrich, Laura S ^a   Cooper, Alan ^a   Haak, Wolfgang ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Max Planck Institute for the Science of Human History ^*  (Germany)

Author keywords

ancient DNA; archaeological sampling; contaminating DNA

Indexed keywords

EID: 85026304421     PISSN: None     EISSN: 20548923     Source Type: Journal    
DOI: 10.1080/20548923.2016.1258824     Document Type: Review

References (146)

1. Adler, C. J., K., Dobney, L. S., Weyrich, J., Kaidonis, A. W., Walker, W., Haak, C. J. A., Bradshaw, et al. 2013. ‘Sequencing Ancient Calcified Dental Plaque Shows Changes in Oral Microbiota with Dietary Shifts of the Neolithic and Industrial Revolutions’. Nature Genetics 45 (4): 450–55. doi: 10.1038/ng.2536
2. Allard, M. W., D., Young, and Y., Huyen. 1995. ‘Detecting Dinosaur DNA’. Science 268 (5214): 1192–1192. doi: 10.1126/science.7761840
3. Allentoft, M. E., 2013. ‘Recovering Samples for Ancient DNA Research—guidelines for the Field Archaeologist’. Antiquity 87 (338): http://antiquity.ac.uk/projgall/allentoft338/.
4. Allentoft, M. E., M., Collins, D., Harker, J., Haile, C. L., Oskam, M. L., Hale, P. F., Campos, et al. 2012. ‘The Half-Life of DNA in Bone: Measuring Decay Kinetics in 158 Dated Fossils’. Proceedings of the Royal Society of London. Series B, Biological Sciences 279 (1748): 4724–33. doi: 10.1098/rspb.2012.1745
5. Allentoft, M. E., M., Sikora, K.-G., Sjogren, S., Rasmussen, M., Rasmussen, J., Stenderup, P. B., Damgaard, et al. 2015. ‘Population Genomics of Bronze Age Eurasia’. Nature 522 (7555): 167–72. doi: 10.1038/nature14507
6. Austin, J. J., A. B., Smith, and R. H., Thomas. 1997. ‘Palaeontology in a Molecular World: The Search for Authentic Ancient DNA’. Trends in Ecology & Evolution 12 (8): 303–6. doi: 10.1016/S0169-5347(97)01102-6
7. Avila-Arcos, M. C., E., Cappellini, J. A., Romero-Navarro, N., Wales, J. V., Moreno-Mayar, M., Rasmussen, S. L., Fordyce, et al. 2011. ‘Application and Comparison of Large-Scale Solution-Based DNA Capture-Enrichment Methods on Ancient DNA’. Scientific Reports 1: 74. doi: 10.1038/srep00074
8. Bengtsson, C. F., M. E., Olsen, L. Y., Brandt, M. F., Bertelsen, E., Willerslev, D. J., Tobin, A. S., Wilson, and M. T. P., Gilbert. 2012. ‘DNA from Keratinous Tissue, Part I: Hair and Nail’. Annals of Anatomy 194 (1): 17–25. doi: 10.1016/j.aanat.2011.03.013
9. Bolnick, D. A., H. M., Bonine, J., Mata-Miguez, B. M., Kemp, M. H., Snow, and S. A., LeBlanc. 2012. ‘Nondestructive Sampling of Human Skeletal Remains Yields Ancient Nuclear and Mitochondrial DNA’. American Journal of Physical Anthropology 147 (2): 293–300. doi: 10.1002/ajpa.21647
10. Bos, K. I., K. M., Harkins, A., Herbig, M., Coscolla, N., Weber, I., Comas, S. A., Forrest, et al. 2014. ‘Pre-Columbian Mycobacterial Genomes Reveal Seals as a Source of New World Human Tuberculosis’. Nature 514 (7523): 494–97. doi: 10.1038/nature13591
11. Bos, K. I., V. J., Schuenemann, G. B., Golding, H. A., Burbano, N., Waglechner, B. K., Coombes, J. B., McPhee, et al. 2011. ‘A Draft Genome of Yersinia Pestis from Victims of the Black Death’. Nature 478 (7370): 506–10. doi: 10.1038/nature10549
12. Brandt, G., A., Szécsényi-Nagy, C., Roth, K. W., Alt, and W., Haak. 2015. ‘Human Paleogenetics of Europe–The Known Knowns and the Known Unknowns’. Journal of Human Evolution 79: 73–92. doi: 10.1016/j.jhevol.2014.06.017
13. Briggs, A. W., U., Stenzel, P. L. F., Johnson, R. E., Green, J., Kelso, K., Prufer, M., Meyer, et al. 2007. ‘Patterns of Damage in Genomic DNA Sequences from a Neandertal’. Proceedings of the National Academy of Sciences of the United States of America 104 (37): 14616–21. doi: 10.1073/pnas.0704665104
14. Briggs, A. W., U., Stenzel, M., Meyer, J., Krause, M., Kircher, and S., Pääbo. 2010. ‘Removal of Deaminated Cytosines and Detection of in Vivo Methylation in Ancient DNA’. Nucleic Acids Research 38 (6): e87. doi: 10.1093/nar/gkp1163
15. Brotherton, P., W., Haak, J., Templeton, G., Brandt, J., Soubrier, C. Jane, Adler, S. M., Richards, et al. 2013. ‘Neolithic Mitochondrial Haplogroup H Genomes and the Genetic Origins of Europeans’. Nature Communications 4: 1764. doi: 10.1038/ncomms2656
16. Brothwell, D. R., and A. M., Pollard. 2001. Handbook of Archaeological Science. Chichester: Wiley-Blackwell.
17. Brown, T. A., and K. A., Brown. 1992. ‘Ancient DNA and the Archaeologist’. Antiquity 66 (250): 10–23. doi: 10.1017/S0003598X0008100X
18. Burbano, H. A., E., Hodges, R. E., Green, A. W., Briggs, J., Krause, M., Meyer, J. M., Good, et al. 2010. ‘Targeted Investigation of the Neandertal Genome by Array-Based Sequence Capture’. Science 328 (5979): 723–25. doi: 10.1126/science.1188046
19. Campos, P. F., O. E., Craig, G., Turner-Walker, E., Peacock, E., Willerslev, and M. T., Gilbert. 2011. ‘DNA in Ancient Bone - Where Is It Located and How Should We Extract It?’ Annals of Anatomy 194 (1): 7–16. doi: 10.1016/j.aanat.2011.07.003
20. Campos, P. F., and T. M., Gilbert. 2012. ‘DNA Extraction from Keratin and Chitin’. Methods in Molecular Biology 840: 43–49. doi: 10.1007/978-1-61779-516-9_6
21. Carpenter, M. L., J. D., Buenrostro, C., Valdiosera, H., Schroeder, M. E., Allentoft, M., Sikora, M., Rasmussen, et al. 2013. ‘Pulling out the 1%: Whole-Genome Capture for the Targeted Enrichment of Ancient DNA Sequencing Libraries’. The American Journal of Human Genetics 93 (5): 852–64. doi: 10.1016/j.ajhg.2013.10.002
22. Castellano, S., G., Parra, F. A., Sánchez-Quinto, F., Racimo, M., Kuhlwilm, M., Kircher, S., Sawyer, et al. 2014. ‘Patterns of Coding Variation in the Complete Exomes of Three Neandertals’. Proceedings of the National Academy of Sciences of the United States of America 111 (18): 6666–71. doi: 10.1073/pnas.1405138111
23. Champlot, S., C., Berthelot, M., Pruvost, E. A., Bennett, T., Grange, and E. M., Geigl. 2010. ‘An Efficient Multistrategy DNA Decontamination Procedure of PCR Reagents for Hypersensitive PCR Applications’. PLoS ONE 5 (9): e13042. doi: 10.1371/journal.pone.0013042
24. Chatters, J. C., D. J., Kennett, Y., Asmerom, B. M., Kemp, V., Polyak, A. N., Blank, P. A., Beddows, et al. 2014. ‘Late Pleistocene Human Skeleton and mtDNA Link Paleoamericans and Modern Native Americans’. Science 344 (6185): 750–54. doi: 10.1126/science.1252619
25. Cooper, A., and H. N., Poinar. 2000. ‘Ancient DNA: Do It Right or Not at All’. Science 289 (5482): 1139. doi: 10.1126/science.289.5482.1139b
26. Dabney, J., M., Knapp, I., Glocke, M. T., Gansauge, A., Weihmann, B., Nickel, C., Valdiosera, et al. 2013. ‘Complete Mitochondrial Genome Sequence of a Middle Pleistocene Cave Bear Reconstructed from Ultrashort DNA Fragments’. Proceedings of the National Academy of Sciences of the United States of America 110 (39): 15758–63. doi: 10.1073/pnas.1314445110
27. Damgaard, P. B., A., Margaryan, H., Schroeder, L., Orlando, E., Willerslev, and M. E., Allentoft. 2015. ‘Improving Access to Endogenous DNA in Ancient Bones and Teeth’. Scientific Reports 5: 11184. doi: 10.1038/srep11184
28. Deguilloux, M.-F., S., Ricaud, R., Leahy, and M.-H., Pemonge. 2011. ‘Analysis of Ancient Human DNA and Primer Contamination: One Step Backward One Step Forward’. Forensic Science International 210 (1-3): 102–9. doi: 10.1016/j.forsciint.2011.02.010
29. Der Sarkissian, C., L., Ermini, H., Jónsson, A. N., Alekseev, E., Crubezy, B., Shapiro, and L., Orlando. 2014. ‘Shotgun Microbial Profiling of Fossil Remains’. Molecular Ecology 23 (7): 1780–98. doi: 10.1111/mec.12690
30. Devault, A. M., G. B., Golding, N., Waglechner, J. M., Enk, M., Kuch, J. H., Tien, M., Shi, et al. 2014a. ‘Second-Pandemic Strain of Vibrio Cholerae from the Philadelphia Cholera Outbreak of 1849’. N Engl J Med 370: 334–40. doi: 10.1056/NEJMoa1308663
31. Devault, A. M., K., McLoughlin, C., Jaing, S., Gardner, T. M., Porter, J. M., Enk, J., Thissen, et al. 2014b. ‘Ancient Pathogen DNA in Archaeological Samples Detected with a Microbial Detection Array’. Scientific Reports 4: 4245. doi: 10.1038/srep04245
32. Enk, J. M., A. M., Devault, M., Kuch, Y. E., Murgha, J.-M., Rouillard, and H. N., Poinar. 2014. ‘Ancient Whole Genome Enrichment Using Baits Built from Modern DNA’. Molecular Biology and Evolution 31 (5): 1292–94. doi: 10.1093/molbev/msu074
33. Ermini, L., C. Der, Sarkissian, E., Willerslev, and L., Orlando. 2015. ‘Major Transitions in Human Evolution Revisited: A Tribute to Ancient DNA’. Journal of Human Evolution 79: 4–20. doi: 10.1016/j.jhevol.2014.06.015
34. Fehren-Schmitz, L., B., Llamas, S., Lindauer, E., Tomasto-Cagigao, S., Kuzminsky, N., Rohland, F. R., Santos, et al. 2015. ‘A Re-Appraisal of the Early Andean Human Remains from Lauricocha in Peru’. PLoS ONE 10 (6): e0127141. doi: 10.1371/journal.pone.0127141
35. Fortea, J., M., de la Rasilla, A., Garcia-Tabernero, E., Gigli, A., Rosas, and C., Lalueza-Fox. 2008. ‘Excavation Protocol of Bone Remains for Neandertal DNA Analysis in El Sidron Cave (Asturias, Spain)’. Journal of Human Evolution 55 (2): 353–57. doi: 10.1016/j.jhevol.2008.03.005
36. Fu, Q., M., Hajdinjak, O. T., Moldovan, S., Constantin, S., Mallick, P., Skoglund, N., Patterson, et al. 2015. ‘An Early Modern Human from Romania with a Recent Neanderthal Ancestor’. Nature 524 (7564): 216–19. doi: 10.1038/nature14558
37. Fu, Q., M., Meyer, X., Gao, U., Stenzel, H. A., Burbano, J., Kelso, and S., Pääbo. 2013a. ‘DNA Analysis of an Early Modern Human from Tianyuan Cave, China’. Proceedings of the National Academy of Sciences of the United States of America 110 (6): 2223–27. doi: 10.1073/pnas.1221359110
38. Fu, Q., A., Mittnik, P. L., Johnson, K., Bos, M., Lari, R., Bollongino, C., Sun, et al. 2013b. ‘A Revised Timescale for Human Evolution Based on Ancient Mitochondrial Genomes’. Current Biology 23 (7): 553–59. doi: 10.1016/j.cub.2013.02.044
39. Fu, Q., C., Posth, M., Hajdinjak, M., Petr, S., Mallick, D., Fernandes, A., Furtwängler, et al. 2016. ‘The Genetic History of Ice Age Europe’. Nature 534 (7606): 200–205.
40. Gallego Llorente, M., E. R., Jones, A., Eriksson, V., Siska, K. W., Arthur, J. W., Arthur, M. C., Curtis, et al. 2015. ‘Ancient Ethiopian Genome Reveals Extensive Eurasian Admixture in Eastern Africa’. Science 350 (6262): 820–22. doi: 10.1126/science.aad2879
41. Gallego Llorente, M., E. R., Jones, A., Eriksson, V., Siska, K. W., Arthur, J. W., Arthur, M. C., Curtis, et al. 2016. ‘Erratum for the Report “Ancient Ethiopian Genome Reveals Extensive Eurasian Admixture in Eastern Africa” (previously Titled “Ancient Ethiopian Genome Reveals Extensive Eurasian Admixture throughout the African Continent”) by M. Gallego Llorente, E. R. Jones, A. Eriksson, V. Siska, K. W. Arthur, J. W. Arthur, M. C. Curtis, J. T. Stock, M. Coltorti, P. Pieruccini, S. Stretton, F. Brock, T. Higham, Y. Park, M. Hofreiter, D. G. Bradley, J. Bhak, R. Pinhasi, A. Manica’. Science 351 (6275): aaf3945. doi: 10.1126/science.aaf3945
42. Gamba, C., K., Hanghøj, C., Gaunitz, A. H., Alfarhan, S. A., Alquraishi, K. A. S., Al-Rasheid, D., Bradley, and L., Orlando. 2015. ‘Comparing the Performance of Three Ancient DNA Extraction Methods for High-Throughput Sequencing’. Molecular Ecology Resources 16 (2): 459–69. doi: 10.1111/1755-0998.12470
43. Gamba, C., E. R., Jones, M. D., Teasdale, R. L., McLaughlin, G., Gonzalez-Fortes, V., Mattiangeli, L., Domboróczki, et al. 2014. ‘Genome Flux and Stasis in a Five Millennium Transect of European Prehistory’. Nature Communications 5: 5257. doi: 10.1038/ncomms6257
44. Gansauge, M.-T., and M., Meyer. 2014. ‘Selective Enrichment of Damaged DNA Molecules for Ancient Genome Sequencing’. Genome Research 24 (9): 1543–49. doi: 10.1101/gr.174201.114
45. Garcia-Garcera, M., E., Gigli, F., Sanchez-Quinto, O., Ramirez, F., Calafell, S., Civit, and C., Lalueza-Fox. 2011. ‘Fragmentation of Contaminant and Endogenous DNA in Ancient Samples Determined by Shotgun Sequencing; Prospects for Human Palaeogenomics’. PLoS ONE 6 (8): e24161. doi: 10.1371/journal.pone.0024161
46. Gilbert, M. T. P., 2014. ‘Yersinia Pestis: One Pandemic, Two Pandemics, Three Pandemics, More?’ The Lancet Infectious Diseases 14 (4): 264–65. doi: 10.1016/S1473-3099(14)70002-7
47. Gilbert, M. T. P., H. J., Bandelt, M., Hofreiter, and I., Barnes. 2005a. ‘Assessing Ancient DNA Studies’. Trends in Ecology & Evolution 20 (10): 541–44. doi: 10.1016/j.tree.2005.07.005
48. Gilbert, M. T. P., D. L., Jenkins, A., Gotherstrom, N., Naveran, J. J., Sanchez, M., Hofreiter, P. F., Thomsen, et al. 2008. ‘DNA from Pre-Clovis Human Coprolites in Oregon, North America’. Science 320 (5877): 786–89. doi: 10.1126/science.1154116
49. Gilbert, M. T. P., L., Rudbeck, E., Willerslev, A. J., Hansen, C., Smith, K. E. H., Penkman, K., Prangenberg, et al. 2005b. ‘Biochemical and Physical Correlates of DNA Contamination in Archaeological Human Bones and Teeth Excavated at Matera, Italy’. Journal of Archaeological Science 32 (5): 785–93. doi: 10.1016/j.jas.2004.12.008
50. Ginolhac, A., M., Rasmussen, M. T., Gilbert, E., Willerslev, and L., Orlando. 2011. ‘mapDamage: Testing for Damage Patterns in Ancient DNA Sequences’. Bioinformatics 27 (15): 2153–55. doi: 10.1093/bioinformatics/btr347
51. Green, R. E., A. W., Briggs, J., Krause, K., Prüfer, H. A., Burbano, M., Siebauer, M., Lachmann, and S., Pääbo. 2009. ‘The Neandertal Genome and Ancient DNA Authenticity’. The EMBO Journal 28 (17): 2494–2502. doi: 10.1038/emboj.2009.222
52. Green, R. E., J., Krause, A. W., Briggs, T., Maricic, U., Stenzel, M., Kircher, N., Patterson, et al. 2010. ‘A Draft Sequence of the Neandertal Genome’. Science 328 (5979): 710–22. doi: 10.1126/science.1188021
53. Green, R. E., J., Krause, S. E., Ptak, A. W., Briggs, M. T., Ronan, J. F., Simons, L., Du, et al. 2006. ‘Analysis of One Million Base Pairs of Neanderthal DNA’. Nature 444 (7117): 330–36. doi: 10.1038/nature05336
54. Green, R. E., A. S., Malaspinas, J., Krause, A. W., Briggs, P. L., Johnson, C., Uhler, M., Meyer, et al. 2008. ‘A Complete Neandertal Mitochondrial Genome Sequence Determined by High-Throughput Sequencing’. Cell 134 (3): 416–26. doi: 10.1016/j.cell.2008.06.021
55. Haak, W., G., Brandt, H. N., de Jong, C., Meyer, R., Ganslmeier, V., Heyd, C., Hawkesworth, A. W., Pike, H., Meller, and K. W., Alt. 2008. ‘Ancient DNA, Strontium Isotopes, and Osteological Analyses Shed Light on Social and Kinship Organization of the Later Stone Age’. Proceedings of the National Academy of Sciences of the United States of America 105 (47): 18226–31. doi: 10.1073/pnas.0807592105
56. Haak, W., I., Lazaridis, N., Patterson, N., Rohland, S., Mallick, B., Llamas, G., Brandt, et al. 2015. ‘Massive Migration from the Steppe Was a Source for Indo-European Languages in Europe’. Nature 522 (7555): 207–11. doi: 10.1038/nature14317
57. Hagelberg, E., M., Hofreiter, and C., Keyser. 2014. ‘Ancient DNA: The First Three Decades’. Philosophical Transactions of the Royal Society B: Biological Sciences 370 (1660): 20130371–20130371. doi: 10.1098/rstb.2013.0371
58. Haile, J., R., Holdaway, K., Oliver, M., Bunce, M. T., Gilbert, R., Nielsen, K., Munch, S. Y., Ho, B., Shapiro, and E., Willerslev. 2007. ‘Ancient DNA Chronology within Sediment Deposits: Are Paleobiological Reconstructions Possible and Is DNA Leaching a Factor?’ Molecular Biology and Evolution 24 (4): 982–89. doi: 10.1093/molbev/msm016
59. Hebsgaard, M. B., M. J., Phillips, and E., Willerslev. 2005. ‘Geologically Ancient DNA: Fact or Artefact?’ Trends in Microbiology 13 (5): 212–20. doi: 10.1016/j.tim.2005.03.010
60. Hedges, S. B., and M. H., Schweitzer. 1995. ‘Detecting Dinosaur DNA’. Science 268 (5214): 1191–92. doi: 10.1126/science.7761839
61. Helgason, A., S., Pálsson, C., Lalueza-Fox, S., Ghosh, S., Sigurðardóttir, A., Baker, B., Hrafnkelsson, L., Árnadóttir, U., Þorsteinsdóttir, and K., Stefánsson. 2007. ‘A Statistical Approach to Identify Ancient Template DNA’. Journal of Molecular Evolution 65 (1): 92–102. doi: 10.1007/s00239-006-0259-8
62. Henikoff, S. 1995. ‘Detecting Dinosaur DNA’. Science 268 (5214): 1192. doi: 10.1126/science.7761841
63. Herrmann, B., and S., Hummel. 1994. Ancient DNA. New York: Springer-Verlag.
64. Higgins, D., and J. J., Austin. 2013. ‘Teeth as a Source of DNA for Forensic Identification of Human Remains: A Review’. Sci Justice 53 (4): 433–41. doi: 10.1016/j.scijus.2013.06.001
65. Hofreiter, M. 2012. ‘Nondestructive DNA Extraction from Museum Specimens’. Methods in Molecular Biology 840: 93–100. doi: 10.1007/978-1-61779-516-9_13
66. Hofreiter, M., D., Serre, H. N., Poinar, M., Kuch, and S., Pääbo. 2001. ‘Ancient DNA’. Nature Reviews Genetics 2 (5): 353–59. doi: 10.1038/35072071
67. Jenkins, D. L., L. G., Davis, T. W., Stafford Jr., P. F., Campos, B., Hockett, G. T., Jones, L. S., Cummings, et al. 2012. ‘Clovis Age Western Stemmed Projectile Points and Human Coprolites at the Paisley Caves’. Science 337 (6091): 223–28. doi: 10.1126/science.1218443
68. Jónsson, H., A., Ginolhac, M., Schubert, P. L., Johnson, and L., Orlando. 2013. ‘mapDamage2.0: Fast Approximate Bayesian Estimates of Ancient DNA Damage Parameters’. Bioinformatics 29 (13): 1682–84. doi: 10.1093/bioinformatics/btt193
69. Kemp, B. M., J., Lindo, D. A., Bolnick, R. S., Malhi, and J. C., Chatters. 2015. ‘Response to Comment on “Late Pleistocene Human Skeleton and mtDNA Link Paleoamericans and Modern Native Americans”’. Science 347 (6224): 835–835. doi: 10.1126/science.1261188
70. Kemp, B. M., and D. G., Smith. 2005. ‘Use of Bleach to Eliminate Contaminating DNA from the Surface of Bones and Teeth’. Forensic Science International 154 (1): 53–61. doi: 10.1016/j.forsciint.2004.11.017
71. Kircher, M. 2012. ‘Analysis of High-Throughput Ancient DNA Sequencing Data’. Methods in Molecular Biology 840: 197–228. doi: 10.1007/978-1-61779-516-9_23
72. Kircher, M., S., Sawyer, and M., Meyer. 2012. ‘Double Indexing Overcomes Inaccuracies in Multiplex Sequencing on the Illumina Platform’. Nucleic Acids Research 40 (1): e3–e3. doi: 10.1093/nar/gkr771
73. Kirsanow, K., and J., Burger. 2012. ‘Ancient Human DNA’. Annals of Anatomy 194 (1): 121–32. doi: 10.1016/j.aanat.2011.11.002
74. Knapp, M., A. C., Clarke, K. A., Horsburgh, and E. A., Matisoo-Smith. 2012a. ‘Setting the Stage - Building and Working in an Ancient DNA Laboratory’. Annals of Anatomy 194 (1): 3–6. doi: 10.1016/j.aanat.2011.03.008
75. Knapp, M., and M., Hofreiter. 2010. ‘Next Generation Sequencing of Ancient DNA: Requirements, Strategies and Perspectives’. Genes 1 (2): 227–43. doi: 10.3390/genes1020227
76. Knapp, M., C., Lalueza-Fox, and M., Hofreiter. 2015. ‘Re-Inventing Ancient Human DNA’. Investigative Genetics 6 (1): 4. doi: 10.1186/s13323-015-0020-4
77. Knapp, M., M., Stiller, and M., Meyer. 2012b. ‘Generating Barcoded Libraries for Multiplex High-Throughput Sequencing’. Methods in Molecular Biology 840: 155–70. doi: 10.1007/978-1-61779-516-9_19
78. Korlević, P., T., Gerber, M.-T., Gansauge, M., Hajdinjak, S., Nagel, A., Aximu-Petri, and M., Meyer. 2015. ‘Reducing Microbial and Human Contamination in DNA Extractions from Ancient Bones and Teeth’. Biotechniques 59 (2): 87–93. doi: 10.2144/000114320
79. Korneliussen, T. S., A., Albrechtsen, and R., Nielsen. 2014. ‘ANGSD: Analysis of next Generation Sequencing Data’. BMC Bioinformatics 15 (1): 356. doi: 10.1186/s12859-014-0356-4
80. Kousathanas, A., C., Leuenberger, V., Link, C., Sell, J., Burger, and D., Wegmann. 2016. ‘Inferring Heterozygosity from Ancient and Low Coverage Genomes’. bioRxiv, April, 046748.
81. Krause, J., A. W., Briggs, M., Kircher, T., Maricic, N., Zwyns, A., Derevianko, and S., Pääbo. 2010. ‘A Complete mtDNA Genome of an Early Modern Human from Kostenki, Russia’. Current Biology 20 (3): 231–36. doi: 10.1016/j.cub.2009.11.068
82. Lazaridis, I., D., Nadel, G., Rollefson, D. C., Merrett, N., Rohland, S., Mallick, D., Fernandes, et al. 2016. ‘Genomic Insights into the Origin of Farming in the Ancient Near East’. Nature 536 (7617): 419–24. doi: 10.1038/nature19310
83. Leonard, J. A., O., Shanks, M., Hofreiter, E., Kreuz, L., Hodges, W., Ream, R. K., Wayne, and R. C., Fleischer. 2007. ‘Animal DNA in PCR Reagents Plagues Ancient DNA Research’. Journal of Archaeological Science 34 (9): 1361–66. doi: 10.1016/j.jas.2006.10.023
84. Lindahl, T. 1993. ‘Instability and Decay of the Primary Structure of DNA’. Nature 362 (6422): 709–15. doi: 10.1038/362709a0
85. Llamas, B., L., Fehren-Schmitz, G., Valverde, J., Soubrier, S., Mallick, N., Rohland, S., Nordenfelt, et al. 2016. ‘Ancient Mitochondrial DNA Provides High-Resolution Time Scale of the Peopling of the Americas’. Science Advances 2 (4): e1501385. doi: 10.1126/sciadv.1501385
86. Malmstrom, H., E. M., Svensson, M. T. P., Gilbert, E., Willerslev, A., Gotherstrom, and G., Holmlund. 2007. ‘More on Contamination: The Use of Asymmetric Molecular Behavior to Identify Authentic Ancient Human DNA’. Molecular Biology and Evolution 24 (4): 998–1004. doi: 10.1093/molbev/msm015
87. Margulies, M., M., Egholm, W. E., Altman, S., Attiya, J. S., Bader, L. A., Bemben, J., Berka, et al. 2005. ‘Genome Sequencing in Microfabricated High-Density Picolitre Reactors’. Nature 437 (7057): 376–80.
88. Mathieson, I., I., Lazaridis, N., Rohland, S., Mallick, N., Patterson, S. A., Roodenberg, E., Harney, et al. 2015. ‘Genome-Wide Patterns of Selection in 230 Ancient Eurasians’. Nature 528 (7583): 499–503. doi: 10.1038/nature16152
89. Meyer, M., J.-L., Arsuaga, C., de Filippo, S., Nagel, A., Aximu-Petri, B., Nickel, I., Martínez, et al. 2016. ‘Nuclear DNA Sequences from the Middle Pleistocene Sima de Los Huesos Hominins’. Nature 531 (7595): 504–7. doi: 10.1038/nature17405
90. Meyer, M., Q., Fu, A., Aximu-Petri, I., Glocke, B., Nickel, J. L., Arsuaga, I., Martinez, et al. 2014. ‘A Mitochondrial Genome Sequence of a Hominin from Sima de Los Huesos’. Nature 505 (7483): 403–6. doi: 10.1038/nature12788
91. Meyer, M., M., Kircher, M.-T., Gansauge, H., Li, F., Racimo, S., Mallick, J. G., Schraiber, et al. 2012. ‘A High-Coverage Genome Sequence from an Archaic Denisovan Individual’. Science 338 (6104): 222–26. doi: 10.1126/science.1224344
92. Mohandesan, E., S., Prost, and M., Hofreiter. 2012. ‘Case Study: Using a Nondestructive DNA Extraction Method to Generate mtDNA Sequences from Historical Chimpanzee Specimens’. Methods in Molecular Biology 840: 101–10. doi: 10.1007/978-1-61779-516-9_14
93. Muller, R., C. A., Roberts, and T. A., Brown. 2013. ‘Biomolecular Identification of Ancient Mycobacterium Tuberculosis Complex DNA in Human Remains from Britain and Continental Europe’. Am J Phys Anthropol 153 (2): 178–89. doi: 10.1002/ajpa.22417
94. Noonan, J. P., M., Hofreiter, D., Smith, J. R., Priest, N., Rohland, G., Rabeder, J., Krause, J. C., Detter, S., Pääbo, and E. M., Rubin. 2005. ‘Genomic Sequencing of Pleistocene Cave Bears’. Science 309 (5734): 597–99. doi: 10.1126/science.1113485
95. Orlando, L., A., Ginolhac, M., Raghavan, J., Vilstrup, M., Rasmussen, K., Magnussen, K. E., Steinmann, et al. 2011. ‘True Single-Molecule DNA Sequencing of a Pleistocene Horse Bone’. Genome Research 21 (10): 1705–19. doi: 10.1101/gr.122747.111
96. Ou, C. Y., J. L., Moore, and G., Schochetman. 1991. ‘Use of UV Irradiation to Reduce False Positivity in Polymerase Chain-Reaction’. Biotechniques 10 (4): 442–&.
97. Pääbo, S. 1989. ‘Ancient DNA: Extraction, Characterization, Molecular Cloning, and Enzymatic Amplification’. Proceedings of the National Academy of Sciences of the United States of America 86 (6): 1939–43. doi: 10.1073/pnas.86.6.1939
98. Pääbo, S. 2014. ‘The Human Condition—A Molecular Approach’. Cell 157 (1): 216–26. doi: 10.1016/j.cell.2013.12.036
99. Pääbo, S., H., Poinar, D., Serre, V., Jaenicke-Despres, J., Hebler, N., Rohland, M., Kuch, J., Krause, L., Vigilant, and M., Hofreiter. 2004. ‘Genetic Analyses from Ancient DNA’. Annual Review of Genetics 38: 645–79. doi: 10.1146/annurev.genet.37.110801.143214
100. Paijmans, J. L., J., Fickel, A., Courtiol, M., Hofreiter, and D. W., Förster. 2015. ‘Impact of Enrichment Conditions on Cross-Species Capture of Fresh and Degraded DNA’. Molecular Ecology Resources 16 (1): 42–55. doi: 10.1111/1755-0998.12420
101. Peltzer, A., G., Jäger, A., Herbig, A., Seitz, C., Kniep, J., Krause, and K., Nieselt. 2016. ‘EAGER: Efficient Ancient Genome Reconstruction’. Genome Biology 17: 60. doi: 10.1186/s13059-016-0918-z
102. Pilli, E., A., Modi, C., Serpico, A., Achilli, H., Lancioni, B., Lippi, F., Bertoldi, S., Gelichi, M., Lari, and D., Caramelli. 2013. ‘Monitoring DNA Contamination in Handled vs. Directly Excavated Ancient Human Skeletal Remains’. PLoS ONE 8 (1): e52524.
103. Pinhasi, R., D., Fernandes, K., Sirak, M., Novak, S., Connell, S., Alpaslan-Roodenberg, F., Gerritsen, et al. 2015. ‘Optimal Ancient DNA Yields from the Inner Ear Part of the Human Petrous Bone’. PLoS ONE 10 (6): e0129102. doi: 10.1371/journal.pone.0129102
104. Poinar, H. N., 2003. ‘The Top 10 List: Criteria of Authenticity for DNA from Ancient and Forensic Samples’. International Congress Series 1239: 575–79. doi: 10.1016/S0531-5131(02)00624-6
105. Posth, C., G., Renaud, A., Mittnik, D. G., Drucker, H., Rougier, C., Cupillard, F., Valentin, et al. 2016. ‘Pleistocene Mitochondrial Genomes Suggest a Single Major Dispersal of Non-Africans and a Late Glacial Population Turnover in Europe’. Current Biology 26 (6): 827–33. doi: 10.1016/j.cub.2016.01.037
106. Prüfer, K., and M., Meyer. 2015. ‘Comment on “Late Pleistocene Human Skeleton and mtDNA Link Paleoamericans and Modern Native Americans”’. Science 347 (6224): 835–835. doi: 10.1126/science.1260617
107. Prüfer, K., F., Racimo, N., Patterson, F., Jay, S., Sankararaman, S., Sawyer, A., Heinze, et al. 2014. ‘The Complete Genome Sequence of a Neanderthal from the Altai Mountains’. Nature 505 (7481): 43–49. doi: 10.1038/nature12886
108. Pruvost, M., R., Schwarz, V. B., Correia, S., Champlot, S., Braguier, N., Morel, Y., Fernandez-Jalvo, T., Grange, and E. M., Geigl. 2007. ‘Freshly Excavated Fossil Bones Are Best for Amplification of Ancient DNA’. Proceedings of the National Academy of Sciences of the United States of America 104 (3): 739–44. doi: 10.1073/pnas.0610257104
109. Racimo, F., G., Renaud, and M., Slatkin. 2016. ‘Joint Estimation of Contamination, Error and Demography for Nuclear DNA from Ancient Humans’. PLOS Genet 12 (4): e1005972. doi: 10.1371/journal.pgen.1005972
110. Raff, J. A., D. A., Bolnick, J., Tackney, and D. H., O’Rourke. 2011. ‘Ancient DNA Perspectives on American Colonization and Population History’. American Journal of Physical Anthropology 146 (4): 503–14. doi: 10.1002/ajpa.21594
111. Raff, J. A., D. C., Cook, and F., Kaestle. 2006. ‘Tuberculosis in the New World: A Study of Ribs from the Schild Mississippian Population, West-Central Illinois’. Memorias Do Instituto Oswaldo Cruz 101: 25–27. doi: 10.1590/S0074-02762006001000005
112. Rasmussen, M., X., Guo, Y., Wang, K. E., Lohmueller, S., Rasmussen, A., Albrechtsen, L., Skotte, et al. 2011. ‘An Aboriginal Australian Genome Reveals Separate Human Dispersals into Asia’. Science 334 (6052): 94–98. doi: 10.1126/science.1211177
113. Rasmussen, M., Y., Li, S., Lindgreen, J. S., Pedersen, A., Albrechtsen, I., Moltke, M., Metspalu, et al. 2010. ‘Ancient Human Genome Sequence of an Extinct Palaeo-Eskimo’. Nature 463 (7282): 757–62. doi: 10.1038/nature08835
114. Renaud, G., V., Slon, A. T., Duggan, and J., Kelso. 2015. ‘Schmutzi: Estimation of Contamination and Endogenous Mitochondrial Consensus Calling for Ancient DNA’. Genome Biology 16 (1): 224. doi: 10.1186/s13059-015-0776-0
115. Rohland, N., E., Harney, S., Mallick, S., Nordenfelt, and D., Reich. 2014. ‘Partial Uracil-DNA-Glycosylase Treatment for Screening of Ancient DNA’. Philosophical Transactions of the Royal Society B: Biological Sciences 370 (1660): 20130624. doi: 10.1098/rstb.2013.0624
116. Salamon, M., N., Tuross, B., Arensburg, and S., Weiner. 2005. ‘Relatively Well Preserved DNA Is Present in the Crystal Aggregates of Fossil Bones’. Proceedings of the National Academy of Sciences of the United States of America 102 (39): 13783–88. doi: 10.1073/pnas.0503718102
117. Sampietro, M. L., M. T. P., Gilbert, O., Lao, D., Caramelli, M., Lari, J., Bertranpetit, and C., Lalueza-Fox. 2006. ‘Tracking down Human Contamination in Ancient Human Teeth’. Molecular Biology and Evolution 23 (9): 1801–7. doi: 10.1093/molbev/msl047
118. Sawyer, S., J., Krause, K., Guschanski, V., Savolainen, and S., Pääbo. 2012. ‘Temporal Patterns of Nucleotide Misincorporations and DNA Fragmentation in Ancient DNA’. PLoS ONE 7 (3): e34131. doi: 10.1371/journal.pone.0034131
119. Schubert, M., A., Ginolhac, S., Lindgreen, J. F., Thompson, K. A., Al-Rasheid, E., Willerslev, A., Krogh, and L., Orlando. 2012. ‘Improving Ancient DNA Read Mapping against Modern Reference Genomes’. BMC Genomics 13 (1): 178. doi: 10.1186/1471-2164-13-178
120. Schuenemann, V. J., K., Bos, S., Dewitte, S., Schmedes, J., Jamieson, A., Mittnik, S., Forrest, et al. 2011. ‘Targeted Enrichment of Ancient Pathogens Yielding the pPCP1 Plasmid of Yersinia Pestis from Victims of the Black Death’. Proceedings of the National Academy of Sciences of the United States of America 108 (38): E746–52. doi: 10.1073/pnas.1105107108
121. Schuenemann, V. J., P., Singh, T. A., Mendum, B., Krause-Kyora, G., Jäger, K. I., Bos, A., Herbig, et al. 2013. ‘Genome-Wide Comparison of Medieval and Modern Mycobacterium Leprae’. Science 341 (6142): 179–83. doi: 10.1126/science.1238286
122. Seguin-Orlando, A., C., Gamba, C. D., Sarkissian, L., Ermini, G., Louvel, E., Boulygina, A., Sokolov, et al. 2015. ‘Pros and Cons of Methylation-Based Enrichment Methods for Ancient DNA’. Scientific Reports 5: 11826. doi: 10.1038/srep11826
123. Seguin-Orlando, A., M., Schubert, J., Clary, J., Stagegaard, M. T., Alberdi, J. L., Prado, A., Prieto, E., Willerslev, and L., Orlando. 2013. ‘Ligation Bias in Illumina Next-Generation DNA Libraries: Implications for Sequencing Ancient Genomes’. PLoS ONE 8 (10): e78575. doi: 10.1371/journal.pone.0078575
124. Skoglund, P., H., Malmstrom, M., Raghavan, J., Stora, P., Hall, E., Willerslev, M. T., Gilbert, A., Gotherstrom, and M., Jakobsson. 2012. ‘Origins and Genetic Legacy of Neolithic Farmers and Hunter-Gatherers in Europe’. Science 336 (6080): 466–69. doi: 10.1126/science.1216304
125. Skoglund, P., B. H., Northoff, M. V., Shunkov, A. P., Derevianko, S., Pääbo, J., Krause, and M., Jakobsson. 2014. ‘Separating Endogenous Ancient DNA from Modern Day Contamination in a Siberian Neandertal’. Proceedings of the National Academy of Sciences of the United States of America 111 (6): 2229–34. doi: 10.1073/pnas.1318934111
126. Skoglund, P., J., Storå, A., Götherström, and M., Jakobsson. 2013. ‘Accurate Sex Identification of Ancient Human Remains Using DNA Shotgun Sequencing’. Journal of Archaeological Science.
127. Slatkin, M., and F., Racimo. 2016. ‘Ancient DNA and Human History’. Proceedings of the National Academy of Sciences 113 (23): 6380–87. doi: 10.1073/pnas.1524306113
128. Smith, C. I., A. T., Chamberlain, M. S., Riley, A., Cooper, C. B., Stringer, and M. J., Collins. 2001. ‘Neanderthal DNA: Not Just Old but Old and Cold?’ Nature 410 (6830): 771–72. doi: 10.1038/35071177
129. Smith, C. I., A. T., Chamberlain, M. S., Riley, C., Stringer, and M. J., Collins. 2003. ‘The Thermal History of Human Fossils and the Likelihood of Successful DNA Amplification’. Journal of Human Evolution 45 (3): 203–17. doi: 10.1016/S0047-2484(03)00106-4
130. Stone, A. C., A. K., Wilbur, J. E., Buikstra, and C. A., Roberts. 2009. ‘Tuberculosis and Leprosy in Perspective’. Am J Phys Anthropol 140 Suppl 49: 66–94. doi: 10.1002/ajpa.21185
131. Tackney, J. C., B. A., Potter, J., Raff, M., Powers, W. S., Watkins, D., Warner, J. D., Reuther, J. D., Irish, and D. H., O’Rourke. 2015. ‘Two Contemporaneous Mitogenomes from Terminal Pleistocene Burials in Eastern Beringia’. Proceedings of the National Academy of Sciences of the United States of America 112 (45): 13833–38. doi: 10.1073/pnas.1511903112
132. Tito, R. Y., D., Knights, J., Metcalf, A. J., Obregon-Tito, L., Cleeland, F., Najar, B., Roe, et al. 2012. ‘Insights from Characterizing Extinct Human Gut Microbiomes’. PLoS ONE 7 (12): e51146. doi: 10.1371/journal.pone.0051146
133. Tito, R. Y., S., Macmil, G., Wiley, F., Najar, L., Cleeland, C., Qu, P., Wang, et al. 2008. ‘Phylotyping and Functional Analysis of Two Ancient Human Microbiomes’. PLoS ONE 3 (11): e3703. doi: 10.1371/journal.pone.0003703
134. Vilstrup, J. T., A., Seguin-Orlando, M., Stiller, A., Ginolhac, M., Raghavan, S. C. A., Nielsen, J., Weinstock, et al. 2013. ‘Mitochondrial Phylogenomics of Modern and Ancient Equids’. PLoS ONE 8 (2): e55950. doi: 10.1371/journal.pone.0055950
135. Vohr, S. H., C. F., Buen Abad Najar, B., Shapiro, and R. E., Green. 2015. ‘A Method for Positive Forensic Identification of Samples from Extremely Low-Coverage Sequence Data’. BMC Genomics 16: 1034. doi: 10.1186/s12864-015-2241-6
136. Wagner, D. M., J., Klunk, M., Harbeck, A., Devault, N., Waglechner, J. W., Sahl, J., Enk, et al. 2014. ‘Yersinia Pestis and the Plague of Justinian 541–543 AD: A Genomic Analysis’. The Lancet Infectious Diseases 14 (4): 319–26. doi: 10.1016/S1473-3099(13)70323-2
137. Wall, J. D., and S. K., Kim. 2007. ‘Inconsistencies in Neanderthal Genomic DNA Sequences’. PLoS Genetics 3 (10): 1862–66. doi: 10.1371/journal.pgen.0030175
138. Warinner, C., J., Hendy, C., Speller, E., Cappellini, R., Fischer, C., Trachsel, J., Arneborg, et al. 2014aa. ‘Direct Evidence of Milk Consumption from Ancient Human Dental Calculus’. Scientific Reports 4: 7104. doi: 10.1038/srep07104
139. Warinner, C., J. F. M., Rodrigues, R., Vyas, C., Trachsel, N., Shved, J., Grossmann, A., Radini, et al. 2014ba. ‘Pathogens and Host Immunity in the Ancient Human Oral Cavity’. Nature Genetics 46 (4): 335–44. doi: 10.1038/ng.2906
140. Warinner, C., C., Speller, and M. J., Collins. 2014bb. ‘A New Era in Palaeomicrobiology: Prospects for Ancient Dental Calculus as a Long-Term Record of the Human Oral Microbiome’. Philosophical Transactions of the Royal Society B: Biological Sciences 370 (1660): 20130376–20130376. doi: 10.1098/rstb.2013.0376
141. Warinner, C., C., Speller, M. J., Collins, and C. M., Lewis Jr. 2015. ‘Ancient Human Microbiomes’. Journal of Human Evolution 79: 125–36. doi: 10.1016/j.jhevol.2014.10.016
142. Weyrich, L. S., K., Dobney, and A., Cooper. 2015. ‘Ancient DNA Analysis of Dental Calculus’. Journal of Human Evolution, Special Issue: Ancient DNA and Human Evolution, 79: 119–24. doi: 10.1016/j.jhevol.2014.06.018
143. Willerslev, E., and A., Cooper. 2005. ‘Ancient DNA’. Proceedings of the Royal Society of London. Series B, Biological Sciences 272 (1558): 3–16. doi: 10.1098/rspb.2004.2813
144. Woodward, N. Weyand, and M., Bunnell. 1994. ‘DNA Sequence from Cretaceous Period Bone Fragments’. Science 266 (5188): 1229–32. doi: 10.1126/science.7973705
145. Yang, D. Y., and K., Watt. 2005. ‘Contamination Controls When Preparing Archaeological Remains for Ancient DNA Analysis’. Journal of Archaeological Science 32 (3): 331–36. doi: 10.1016/j.jas.2004.09.008
146. Zischler, H., M., Hoss, O., Handt, A., von Haeseler, A. C., van der Kuyl, and J., Goudsmit. 1995. ‘Detecting Dinosaur DNA’. Science 268 (5214): 1192–93. doi: 10.1126/science.7605504