The future of ancient DNA: Technical advances and conceptual shifts

BioEssays

Volumn 37, Issue 3, 2015, Pages 284-293

  Hofreiter, Michael ^a,b   Paijmans, Johanna L A ^a   Goodchild, Helen ^b   Speller, Camilla F ^b   Barlow, Axel ^a   Fortes, Gloria G ^a   Thomas, Jessica A ^b   Ludwig, Arne ^c   Collins, Matthew J ^b  

^a UNIVERSITY OF POTSDAM   (Germany)

^b UNIVERSITY OF YORK   (United Kingdom)

^c LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

Author keywords

Ancient DNA; Hybridisation capture; Multi locus data; Next generation sequencing (NGS); Palaeogenomics; Population genomics

Indexed keywords

DNA;

ARTICLE; BIOINFORMATICS; CLINICAL RESEARCH; CONCEPTUAL FRAMEWORK; CORRELATIONAL STUDY; DNA HYBRIDIZATION; DNA SEQUENCE; GENOMICS; HUMAN; NEXT GENERATION SEQUENCING; NONHUMAN; PALAEOGENOMICS; POPULATION DYNAMICS; ANIMAL; DNA DAMAGE; GENETICS; GENOME; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; MULTILOCUS SEQUENCE TYPING; TEMPERATURE;

ANIMALS; DNA; DNA DAMAGE; GENOME; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MULTILOCUS SEQUENCE TYPING; TEMPERATURE;

EID: 84925460540     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400160     Document Type: Article

References (112)

1. Pääbo S. 1985. Preservation of DNA in ancient Egyptian mummies. J Archaeol Sci 12: 411-7.
2. Higuchi R, Bowman B, Freiberger M, Ryder OA, et al. 1984. DNA sequences from the quagga, an extinct member of the horse family. Nature 312: 282-4.
3. Pääbo S. 1985. Molecular cloning of ancient Egyptian mummy DNA. Nature 314: 644-5.
4. Leonard JA, Rohland N, Glaberman S, Fleischer RC, et al. 2005. A rapid loss of stripes: the evolutionary history of the extinct quagga. Biol Lett 1: 291-5.
5. Pääbo S, Wilson AC. 1988. Polymerase chain reaction reveals cloning artefacts. Nature 334: 387-8.
6. Pääbo S, Poinar H, Serre D, Jaenicke-Després V, et al. 2004. Genetic analyses from ancient DNA. Annu Rev Genet 38: 645-79.
7. Gilbert MTP, Bandelt H-J, Hofreiter M, Barnes I. 2005. Assessing ancient DNA studies. Trends Ecol Evol 20: 541-4.
8. Lambert DM, Ritchie PA, Millar CD, Holland B, et al. 2002. Rates of evolution in ancient DNA from Adélie penguins. Science 295: 2270-3.
9. Hofreiter M, Serre D, Poinar HN, Kuch M, et al. 2001. Ancient DNA. Nat Rev Genet 2: 353-9.
10. Paijmans JLA, Gilbert MTP, Hofreiter M. 2013. Mitogenomic analyses from ancient DNA. Mol Phylogenet Evol 69: 404-16.
11. Huynen L, Millar CD, Lambert DM. 2012. Resurrecting ancient animal genomes: the extinct moa and more. BioEssays 34: 661-9.
12. Gilbert MTP, Cuccui J, White W, Lynnerup N, et al. 2004. Absence of Yersinia pestis-specific DNA in human teeth from five European excavations of putative plague victims. Microbiology 150: 341-54.
13. Shapiro B, Rambaut A, Gilbert MTP. 2006. No proof that typhoid caused the Plague of Athens (a reply to Papagrigorakis et al.). Int J Infect Dis 10: 334-5.
14. Margulies M, Egholm M, Altman WE, Attiya S, et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-80.
15. Mamanova L, Coffey AJ, Scott CE, Kozarewa I, et al. 2010. Target-enrichment strategies for next-generation sequencing. Nat Meth 7: 111-8.
16. Briggs AW, Good JM, Green RE, Krause J, et al. 2009. Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science 325: 318-21.
17. Maricic T, Whitten M, Pääbo S. 2010. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One 5: e14004.
18. Carpenter ML, Buenrostro JD, Valdiosera C, Schroeder H, et al. 2013. Pulling out the 1%: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am J Hum Genet 93: 852-64.
19. Enk JM, Devault AM, Kuch M, Murgha YE, et al. 2014. Ancient whole genome enrichment using baits built from modern DNA. Mol Biol Evol 31: 1292-4.
20. Dabney J, Knapp M, Glocke I, Gansauge M-T, et al. 2013. Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc Natl Acad Sci USA 110: 15758-63.
21. Brotherton P, Endicott P, Sanchez JJ, Beaumont M, et al. 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: 5717-28.
22. Briggs AW, Stenzel U, Meyer M, Krause J, et al. 2010. Removal of deaminated cytosines and detection of in vivo methylation in ancient DNA. Nucleic Acids Res 38: e87.
23. Briggs AW, Stenzel U, Johnson PLF, Green RE, et al. 2007. Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci USA 104: 14616-21.
24. Orlando L, Ginolhac A, Raghavan M, Vilstrup J, et al. 2011. True single-molecule DNA sequencing of a Pleistocene horse bone. Genome Res 21: 1705-19.
25. Sawyer S, Krause J, Guschanski K, Savolainen V, et al. 2012. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS One 7: e34131.
26. Ginolhac A, Rasmussen M, Gilbert MTP, Willerslev E, et al. 2011. mapDamage: testing for damage patterns in ancient DNA sequences. Bioinformatics 27: 2153-5.
27. Jónsson H, Ginolhac A, Schubert M, Johnson PLF, et al. 2013. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29: 1682-4.
28. Smith O, Clapham A, Rose P, Liu Y, et al. 2014. A complete ancient RNA genome: identification, reconstruction and evolutionary history of archaeological Barley Stripe Mosaic Virus. Sci Rep 4: 4003.
29. Gansauge M-T, Meyer M. 2014. Selective enrichment of damaged DNA molecules for ancient genome sequencing. Genome Res 24: 1543-9.
30. Skoglund P, Northoff BH, Shunkov MV, Derevianko AP, et al. 2014. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal. Proc Natl Acad Sci USA 111: 2229-34.
31. Poinar HN, Höss M, Bada JL, Pääbo S. 1996. Amino acid racemization and the preservation of ancient DNA. Science 272: 864-6.
32. Collins MJ, Penkman KEH, Rohland N, Shapiro B, et al. 2009. Is amino acid racemization a useful tool for screening for ancient DNA in bone? Proc R Soc B Biol Sci 276: 2971-7.
33. Allentoft ME, Collins M, Harker D, Haile J, et al. 2012. The half-life of DNA in bone: measuring decay kinetics in 158 dated fossils. Proc R Soc B Biol Sci 279: 4724-33.
34. Hughey JR, Braga JC, Aguirre J, Woelkerling WJ, et al. 2008. Analysis of ancient DNA from fossil corallines (Corallinales, Rhodophyta). J Phycol 44: 374-83.
35. Hijmans RJ, Cameron S, Parra J, Jones PG, et al. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 1965-78.
36. Bintanja R, van de Wal RSW, Oerlemans J. 2005. Modelled atmospheric temperatures and global sea levels over the past million years. Nature 437: 125-8.
37. Rasmussen M, Anzick SL, Waters MR, Skoglund P, et al. 2014. The genome of a Late Pleistocene human from a Clovis burial site in western Montana. Nature 506: 225-9.
38. Rohland N, Hofreiter M. 2007. Comparison and optimization of ancient DNA extraction. BioTechniques 42: 343-52.
39. Bouwman AS, Brown TA. 2002. Comparison between silica-based methods for the extraction of DNA from human bones from 18th to Mid-19th century London. Anc Biomol 4: 173-8.
40. Yang DY, Eng B, Waye JS, Dudar JC, et al. 1998. Improved DNA extraction from ancient bones using silica-based spin columns. Am J Phys Anthropol 105: 539-43.
41. Meyer M, Fu Q, Aximu-Petri A, Glocke I, et al. 2013. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505: 403-6.
42. Orlando L. 2014. A 400, 000-year-old mitochondrial genome questions phylogenetic relationships amongst archaic hominins. BioEssays 36: 598-605.
43. Orlando L, Ginolhac A, Zhang G, Froese D, et al. 2013. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499: 74-8.
44. Geigl E-M. 2002. On the circumstances surrounding the preservation and analysis of very old DNA. Archaeometry 44: 337-42.
45. Barta JL, Monroe C, Teisberg JE, Winters M, et al. 2014. One of the key characteristics of ancient DNA, low copy number, may be a product of its extraction. J Archaeol Sci 46: 281-9.
46. Gilbert MTP, Tomsho LP, Rendulic S, Packard M, et al. 2007. Whole-genome shotgun sequencing of mitochondria from ancient hair shafts. Science 317: 1927-30.
47. Rasmussen M, Li Y, Lindgreen S, Pedersen JS, et al. 2010. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463: 757-62.
48. Gamba C, Jones ER, Teasdale MD, McLaughlin RL, et al. 2014. Genome flux and stasis in a five millennium transect of European prehistory. Nat Commun 4: 5257.
49. Noonan JP, Hofreiter M, Smith D, Priest JR, et al. 2005. Genomic sequencing of Pleistocene cave bears. Science 309: 597-9.
50. Green RE, Krause J, Ptak SE, Briggs AW, et al. 2006. Analysis of one million base pairs of Neanderthal DNA. Nature 444: 330-6.
51. Briggs AW, Heyn P. 2012. Preparation of next-generation sequencing libraries from damaged DNA. In Shapiro B, Hofreiter M, eds; Ancient DNA. New York: Humana Press. pp. 143-54.
52. Maricic T, Pääbo S. 2009. Optimization of 454 sequencing library preparation from small amounts of DNA permits sequence determination of both DNA strands. BioTechniques 46: 51-2, 54-7.
53. Bennett EA, Massilani D, Lizzo G, Daligault J, et al. 2014. Library construction for ancient genomics: single strand or double strand? BioTechniques 56: 289-90, 292-6, 298, passim.
54. Meyer M, Kircher M, Gansauge M-T, Li H, et al. 2012. A high-coverage genome sequence from an archaic Denisovan individual. Science 338: 222-6.
55. Gansauge M-T, Meyer M. 2013. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat Protoc 8: 737-48.
56. Branton D, Deamer DW, Marziali A, Bayley H, et al. 2008. The potential and challenges of nanopore sequencing. Nat Biotechnol 26: 1146-53.
57. Eid J, Fehr A, Gray J, Luong K, et al. 2009. Real-time DNA sequencing from single polymerase molecules. Science 323: 133-8.
58. Skoglund P, Malmström H, Raghavan M, Storå J, et al. 2012. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336: 466-9.
59. Zhang H, Paijmans JLA, Chang F, Wu X, et al. 2013. Morphological and genetic evidence for early Holocene cattle management in northeastern China. Nat Commun 4: 2755.
60. Burbano HA, Hodges E, Green RE, Briggs AW, et al. 2010. Targeted investigation of the Neandertal genome by array-based sequence capture. Science 328: 723-35.
61. Devault AM, Golding GB, Waglechner N, Enk JM, et al. 2014. Second-pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. N Engl J Med 370: 334-40.
62. Enk J, Rouillard J-M, Poinar H. 2013. Quantitative PCR as a predictor of aligned ancient DNA read counts following targeted enrichment. BioTechniques 55: 300-9.
63. Castellano S, Parra G, Sánchez-Quinto FA, Racimo F, et al. 2014. Patterns of coding variation in the complete exomes of three Neandertals. Proc Natl Acad Sci USA 111: 6666-71.
64. Cosart T, Beja-Pereira A, Chen S, Ng SB, et al. 2011. Exome-wide DNA capture and next generation sequencing in domestic and wild species. BMC Genomics 12: 347.
65. Bi K, Vanderpool D, Singhal S, Linderoth T, et al. 2012. Transcriptome-based exon capture enables highly cost-effective comparative genomic data collection at moderate evolutionary scales. BMC Genomics 13: 403.
66. Fortes GG, Speller CF, Hofreiter M, King TE. 2013. Phenotypes from ancient DNA: approaches, insights and prospects. BioEssays 35: 690-5.
67. Elhaik E, Greenspan E, Staats S, Krahn T, et al. 2013. The GenoChip: a new tool for genetic anthropology. Genome Biol Evol 5: 1021-31.
68. Charlier C, Coppieters W, Rollin F, Desmecht D, et al. 2008. Highly effective SNP-based association mapping and management of recessive defects in livestock. Nat Genet 40: 449-54.
69. Martinsohn JT, Ogden R. 2009. FishPopTrace-Developing SNP-based population genetic assignment methods to investigate illegal fishing. Forensic Sci Int Genet Suppl Ser 2: 294-6.
70. Backström N, Fagerberg S, Ellegren H. 2008. Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17: 964-80.
71. Decker JE, Pires JC, Conant GC, McKay SD, et al. 2009. Resolving the evolution of extant and extinct ruminants with high-throughput phylogenomics. Proc Natl Acad Sci USA 106: 18644-9.
72. Nielsen R. 2004. Population genetic analysis of ascertained SNP data. Hum Genomics 1: 218.
73. Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, et al. 2005. Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15: 1496-502.
74. Schubert M, Ginolhac A, Lindgreen S, Thompson JF, et al. 2012. Improving ancient DNA read mapping against modern reference genomes. BMC Genomics 13: 178.
75. Green RE, Malaspinas A-S, Krause J, Briggs AW, et al. 2008. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell 134: 416-26.
76. Hahn C, Bachmann L, Chevreux B. 2013. Reconstructing mitochondrial genomes directly from genomic next-generation sequencing reads-a baiting and iterative mapping approach. Nucleic Acids Res 41: e129.
77. Rajaraman A, Tannier E, Chauve C. 2013. FPSAC: fast phylogenetic scaffolding of ancient contigs. Bioinformatics 29: 2987-94.
78. Haile J, Holdaway R, Oliver K, Bunce M, et al. 2007. Ancient DNA chronology within sediment deposits: are paleobiological reconstructions possible and is DNA leaching a factor? Mol Biol Evol 24: 982-9.
79. Wood DE, Salzberg SL. 2014. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 15: R46.
80. Skoglund P, Sjödin P, Skoglund T, Lascoux M, et al. 2014. Investigating population history using temporal genetic differentiation. Mol Biol Evol 31: 2516-27.
81. Pickrell JK, Pritchard JK. 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet 8: e1002967.
82. Sites JW, Marshall JC. 2004. Operational criteria for delimiting species. Annu Rev Ecol Evol Syst 35: 199-227.
83. Queiroz KD. 2007. Species concepts and species delimitation. Syst Biol 56: 879-86.
84. Reich D, Patterson N, Kircher M, Delfin F, et al. 2011. Denisova admixture and the first modern human dispersals into southeast Asia and Oceania. Am J Hum Genet 89: 516-28.
85. Hellenthal G, Busby GBJ, Band G, Wilson JF, et al. 2014. A genetic atlas of human admixture history. Science 343: 747-51.
86. Pardini AT, Jones CS, Noble LR, Kreiser B, et al. 2001. Sex-biased dispersal of great white sharks. Nature 412: 139-40.
87. Frantz LA, Schraiber JG, Madsen O, Megens H-J, et al. 2013. Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus. Genome Biol 14: R107.
88. Rohde DLT, Olson S, Chang JT. 2004. Modelling the recent common ancestry of all living humans. Nature 431: 562-6.
89. Pickrell J, Reich D. 2014. Towards a new history and geography of human genes informed by ancient DNA. Trends Genet 30: 377-89.
90. Fordyce SL, Ávila-Arcos MC, Rasmussen M, Cappellini E, et al. 2013. Deep sequencing of RNA from ancient maize kernels. PLoS One 8: e50961.
91. Sallon S, Solowey E, Cohen Y, Korchinsky R, et al. 2008. Germination, genetics, and growth of an ancient date seed. Science 320: 1464.
92. Santiago-Rodriguez TM, Patrício AR, Rivera JI, Coradin M, et al. 2014. luxS in bacteria isolated from 25- to 40-million-year-old amber. FEMS Microbiol Lett 350: 117-24.
93. Weyrich LS, Llamas B, Cooper A. 2014. Reply to Santiago-Rodriguez et al.: was luxS really isolated from 25- to 40-million-year-old bacteria? FEMS Microbiol Lett 353: 85-6.
94. Warinner C, Rodrigues JFM, Vyas R, Trachsel C, et al. 2014. Pathogens and host immunity in the ancient human oral cavity. Nat Genet 46: 336-44.
95. Achtman M. 2012. Insights from genomic comparisons of genetically monomorphic bacterial pathogens. Philos Trans R Soc B Biol Sci 367: 860-7.
96. Campana MG, García NR, Rühli FJ, Tuross N. 2014. False positives complicate ancient pathogen identifications using high-throughput shotgun sequencing. BMC Res Notes 7: 111.
97. Warinner C, Speller C, Collins M. 2015. A new era in paleomicrobiology: Prospects for ancient dental calculus as a long-term record of the human oral microbiome. Philos Trans R Soc B Biol Sci, in press, doi: 10.1098/rstb.2013.0376.
98. Adler CJ, Dobney K, Weyrich LS, Kaidonis J, et al. 2013. Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat Genet 45: 450-5.
99. Tito RY, Knights D, Metcalf J, Obregon-Tito AJ, et al. 2012. Insights from characterizing extinct human gut microbiomes. PLoS One 7: e51146.
100. Maixner F, Thomma A, Cipollini G, Widder S, et al. 2014. Metagenomic analysis reveals presence of Treponema denticola in a tissue biopsy of the iceman. PLoS One 9: e99994.
101. Chapman SJ, Hill AVS. 2012. Human genetic susceptibility to infectious disease. Nat Rev Genet 13: 175-88.
102. Thalmann O, Shapiro B, Cui P, Schuenemann VJ, et al. 2013. Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs. Science 342: 871-4.
103. Ludwig A, Pruvost M, Reissmann M, Benecke N, et al. 2009. Coat color variation at the beginning of horse domestication. Science 324: 485.
104. Flink LG, Allen R, Barnett R, Malmström H, et al. 2014. Establishing the validity of domestication genes using DNA from ancient chickens. Proc Natl Acad Sci USA 111: 6184-9.
105. Larson G, Piperno DR, Allaby RG, Purugganan MD, et al. 2014. Current perspectives and the future of domestication studies. Proc Natl Acad Sci USA 111: 6139-46.
106. Tishkoff SA, Reed FA, Ranciaro A, Voight BF, et al. 2007. Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39: 31-40.
107. Itan Y, Powell A, Beaumont MA, Burger J, et al. 2009. The Origins of Lactase Persistence in Europe. PLoS Comput Biol 5: e1000491.
108. Avise JC. 2000. Phylogeography: The History and Formation of Species. Cambridge MA: Harvard University Press.
109. Hauser L, Adcock GJ, Smith PJ, Ramírez JHB, et al. 2002. Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99: 11742-7.
110. Pedersen JS, Valen E, Velazquez AMV, Parker BJ, et al. 2014. Genome-wide nucleosome map and cytosine methylation levels of an ancient human genome. Genome Res 24: 454-66.
111. Smith O, Clapham AJ, Rose P, Liu Y, et al. 2014. Genomic methylation patterns in archaeological barley show de-methylation as a time-dependent diagenetic process. Sci Rep 4: 5559.
112. Gokhman D, Lavi E, Prüfer K, Fraga MF, et al. 2014. Reconstructing the DNA methylation maps of the Neandertal and the Denisovan. Science 344: 523-7.