Molecular genetic aspects of ancient DNA analyses
Abstract
This review article presents molecular genetic aspects of human ancient DNA analyses and use of molecular genetic methods for study of DNA obtained from human archaeological biological materials. In archaeological biological materials, skeletal remains (bones and teeth) are often the only source of ancient DNA and we will focus on these tissues. From the literature reviewed, we will summarise which skeletal elements are most suitable for the investigation of ancient DNA and how to extract the DNA from them. The nature and preservation of ancient DNA will be described as well. However, low amount and degradation of ancient DNA causes several problems, especially when working with ancient human samples that may be contaminated with modern human DNA. To minimise the risk of contamination, several standard precautions are usually adopted and the authenticity of ancient DNA checked. We will pay special attention to these measures. The genetic markers most frequently examined in archaeogenetics and the advantages of new, high-performing sequencing techniques for the development and study of ancient DNA will be described. Using new techniques that may help us retrieve data of better quality and quantity, we can investigate more degraded DNA and thus older archaeological biological materials, thereby obtaining huge amounts of data that require the involvement of experts in the field of bioinformatics. The paper will be completed by the presentation of ancient DNA analyses performed in Slovenia.
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Márquez-Grant N, Webster H, Truesdell J, Fibiger L. Physical anthropology and osteoarchaeology in Europe: History, current trends and challenges. Int J Osteoarchaeol. 2016;26(6):1078–88. https://doi.org/10.1002/oa.2520.
Bouwman A, Rühli F. Archaeogenetics in evolutionary medicine. J Mol Med (Berl). 2016 Sep;94(9):971–7. https://doi.org/10.1007/s00109-016-1438-8 PMID:27289479
Baum DA, Futuyma DJ, Hoekstra HE, Lenski RE, Moore JA, Peichel CL, et al. The Princeton Guide to Evolution. Princeton: Princeton University Press; 2013. pp. 477–9.
Hagelberg E, Quevedo S, Turbon D, Clegg JB. DNA from ancient Easter Islanders. Nature. 1994 May;369(6475):25–6. https://doi.org/10.1038/369025a0 PMID:8164735
Ingman M, Kaessmann H, Pääbo S, Gyllensten U. Mitochondrial genome variation and the origin of modern humans. Nature. 2000 Dec;408(6813):708–13. https://doi.org/10.1038/35047064 PMID:11130070
Sampietro ML, Gilbert MT, Lao O, Caramelli D, Lari M, Bertranpetit J, et al. Tracking down human contamination in ancient human teeth. Mol Biol Evol. 2006 Sep;23(9):1801–7. https://doi.org/10.1093/molbev/msl047 PMID:16809622
Cooper A, Poinar HN. Ancient DNA: do it right or not at all. Science. 2000 Aug;289(5482):1139. https://doi.org/10.1126/science.289.5482.1139b PMID:10970224
Obal M. Uporaba različnih skeletnih elementov za genetsko identifikacijo žrtev druge svetovne vojne [Master’s Thesis]. Ljubljana: M. Obal; 2018.
Ziętkiewicz E, Witt M, Daca P, Zebracka-Gala J, Goniewicz M, Jarząb B, et al. Current genetic methodologies in the identification of disaster victims and in forensic analysis. J Appl Genet. 2012 Feb;53(1):41–60. https://doi.org/10.1007/s13353-011-0068-7 PMID:22002120
Irwin JA, Just RS, Loreille OM, Parsons TJ. Characterization of a modified amplification approach for improved STR recovery from severely degraded skeletal elements. Forensic Sci Int Genet. 2012 Sep;6(5):578–87. https://doi.org/10.1016/j.fsigen.2012.01.010 PMID:22402195
Anderung C, Persson P, Bouwman A, Elburg R, Götherström A. Fishing for ancient DNA. Forensic Sci Int Genet. 2008 Mar;2(2):104–7. https://doi.org/10.1016/j.fsigen.2007.09.004 PMID:19083805
Zupanič Pajnič I. Molekularnogenetska identifikacija skeletnih ostankov. Med Razgl. 2013;52:213–34.
Campos PF, Craig OE, Turner-Walker G, Peacock E, Willerslev E, Gilbert MT. DNA in ancient bone - where is it located and how should we extract it? Ann Anat. 2012 Jan;194(1):7–16. https://doi.org/10.1016/j.aanat.2011.07.003 PMID:21855309
Putkonen MT, Palo JU, Cano JM, Hedman M, Sajantila A. Factors affecting the STR amplification success in poorly preserved bone samples. Investig Genet. 2010 Oct;1(1):9. https://doi.org/10.1186/2041-2223-1-9 PMID:21092342
Higgins D, Austin JJ. Teeth as a source of DNA for forensic identification of human remains: a review. Sci Justice. 2013 Dec;53(4):433–41. https://doi.org/10.1016/j.scijus.2013.06.001 PMID:24188345
Pruvost M, Schwarz R, Correia VB, Champlot S, Braguier S, Morel N, et al. Freshly excavated fossil bones are best for amplification of ancient DNA. Proc Natl Acad Sci USA. 2007 Jan;104(3):739–44. https://doi.org/10.1073/pnas.0610257104 PMID:17210911
Mundorff A, Davoren JM. Examination of DNA yield rates for different skeletal elements at increasing post mortem intervals. Forensic Sci Int Genet. 2014 Jan;8(1):55–63. https://doi.org/10.1016/j.fsigen.2013.08.001 PMID:24315589
Hofreiter M, Serre D, Poinar HN, Kuch M, Pääbo S. Ancient DNA. Nat Rev Genet. 2001 May;2(5):353–9. https://doi.org/10.1038/35072071 PMID:11331901
Kendall C, Høier Eriksen AM, Kontopoulos I, Collins MJ, Turner-Walker G. Diagenesis of archaeological bone and tooth. Paleogeogr Palaeocl. 2018;491:21–37. https://doi.org/10.1016/j.palaeo.2017.11.041.
Mansour H, Krebs O, Sperhake JP, Augustin C, Koehne T, Amling M, et al. Cementum as a source of DNA in challenging forensic cases. J Forensic Leg Med. 2018 Feb;54:76–81. https://doi.org/10.1016/j.jflm.2017.12.015 PMID:29328966
Kemp BM, Smith DG. Use of bleach to eliminate contaminating DNA from the surface of bones and teeth. Forensic Sci Int. 2005 Nov;154(1):53–61. https://doi.org/10.1016/j.forsciint.2004.11.017 PMID:16182949
Coulson-Thomas YM, Norton AL, Coulson-Thomas VJ, Florencio-Silva R, Ali N, Elmrghni S, et al. DNA and bone structure preservation in medieval human skeletons. Forensic Sci Int. 2015 Jun;251:186–94. https://doi.org/10.1016/j.forsciint.2015.04.005 PMID:25912776
Turner-Walker G. The chemical and microbial degradation of bones and teeth. In: Pinhasi R, Mays S: Advances in Human Palaeopathology. John Wiley and Sonds LTD, 2008:1–29.
Siriboonpiputtana T, Rinthachai T, Shotivaranon J, Peonim V, Rerkamnuaychoke B. Forensic genetic analysis of bone remain samples. Forensic Sci Int. 2018 Mar;284:167–75. https://doi.org/10.1016/j.forsciint.2017.12.045 PMID:29408726
Miloš A, Selmanović A, Smajlović L, Huel RL, Katzmarzyk C, Rizvić A, et al. Success rates of nuclear short tandem repeat typing from different skeletal elements. Croat Med J. 2007 Aug;48(4):486–93. PMID:17696303
Prinz M, Carracedo A, Mayr WR, Morling N, Parsons TJ, Sajantila A, et al.; International Society for Forensic Genetics. DNA Commission of the International Society for Forensic Genetics (ISFG): recommendations regarding the role of forensic genetics for disaster victim identification (DVI). Forensic Sci Int Genet. 2007 Mar;1(1):3–12. https://doi.org/10.1016/j.fsigen.2006.10.003 PMID:19083722
Edson SM, Ross JP, Coble MD, Parsons TJ, Barritt SM. Naming the Dead - Confronting the Realities of Rapid Identification of Degraded Skeletal Remains. Forensic Sci Rev. 2004 Jan;16(1):63–90. PMID:26256813
Mundorff AZ, Bartelink EJ, Mar-Cash E. DNA preservation in skeletal elements from the World Trade Center disaster: recommendations for mass fatality management. J Forensic Sci. 2009 Jul;54(4):739–45. https://doi.org/10.1111/j.1556-4029.2009.01045.x PMID:19486445
Andronowski JM, Mundorff AZ, Pratt IV, Davoren JM, Cooper DM. Evaluating differential nuclear DNA yield rates and osteocyte numbers among human bone tissue types: A synchrotron radiation micro-CT approach. Forensic Sci Int Genet. 2017 May;28:211–8. https://doi.org/10.1016/j.fsigen.2017.03.002 PMID:28315820
Hines DZ, Vennemeyer M, Amory S, Huel RL, Hanson I, Katzmarzyk C, et al. Prioritizing sampling of bone and teeth for DNA analysis in commingled cases. In: Adams BJ, Byrd JE, editors. Commingled Human Remains: Methods in Recovery, Analysis, and Identification. Oxford: Elsevier Science; 2014. pp. 275–305. https://doi.org/10.1016/B978-0-12-405889-7.00013-7.
Pilli E, Vai S, Caruso MG, D’Errico G, Berti A, Caramelli D. Neither femur nor tooth: petrous bone for identifying archaeological bone samples via forensic approach. Forensic Sci Int. 2018 Feb;283:144–9. https://doi.org/10.1016/j.forsciint.2017.12.023 PMID:29301114
Hansen HB, Damgaard PB, Margaryan A, Stenderup J, Lynnerup N, Willerslev E, et al. Comparing Ancient DNA Preservation in Petrous Bone and Tooth Cementum. PLoS One. 2017 Jan;12(1):e0170940. https://doi.org/10.1371/journal.pone.0170940 PMID:28129388
Pinhasi R, Fernandes D, Sirak K, Novak M, Connell S, Alpaslan-Roodenberg S, et al. Optimal ancient DNA yields from the inner ear part of the human petrous bone. PLoS One. 2015;18:10(6):e0129102.
Gamba C, Jones ER, Teasdale MD, McLaughlin RL, Gonzalez-Fortes G, Mattiangeli V, et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat Commun. 2014 Oct;5(1):5257. https://doi.org/10.1038/ncomms6257 PMID:25334030
Jamieson A, Bader S. A guide to forensic DNA profiling, Wiley, Hoboken, NJ, 2016:5-6, 15-18, 32-34, 37-38, 108-109, 115-117.
Butler JM. Forensic DNA Typing: Biology, Technology, and Genetics of STR Markers, 2nd edition, Elsevier, ZDA, 2005:86-90.
Anderson S, Bankier AT, Barrell BG, de Bruijn MH, Coulson AR, Drouin J, et al. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr;290(5806):457–65. https://doi.org/10.1038/290457a0 PMID:7219534
Fisher DL, Holland MM, Mitchell L, Sledzik PS, Wilcox AW, Wadhams M, et al. Extraction, evaluation, and amplification of DNA from decalcified and undecalcified United States Civil War bone. J Forensic Sci. 1993 Jan;38(1):60–8. https://doi.org/10.1520/JFS13376J PMID:8426158
Holland MM, Fisher DL, Mitchell LG, Rodriquez WC, Canik JJ, Merril CR, et al. Mitochondrial DNA sequence analysis of human skeletal remains: identification of remains from the Vietnam War. J Forensic Sci. 1993 May;38(3):542–53. https://doi.org/10.1520/JFS13439J PMID:8515208
Hopwood AJ, Mannucci A, Sullivan KM. DNA typing from human faeces. Int J Legal Med. 1996;108(5):237–43. https://doi.org/10.1007/BF01369817 PMID:8721422
Pääbo S, Poinar H, Serre D, Jaenicke-Despres V, Hebler J, Rohland N, et al. Genetic analyses from ancient DNA. Annu Rev Genet. 2004;38(1):645–79. https://doi.org/10.1146/annurev.genet.37.110801.143214 PMID:15568989
Palo JU, Hedman M, Söderholm N, Sajantila A. Repatriation and identification of the Finnish World War II soldiers. Croat Med J. 2007 Aug;48(4):528–35. PMID:17696308
Zupanič Pajnič I, Gornjak Pogorelc B, Balažic J. Molecular genetic identification of skeletal remains from the Second World War Konfin I mass grave in Slovenia. Int J Legal Med. 2010 Jul;124(4):307–17. https://doi.org/10.1007/s00414-010-0431-y PMID:20217112
Zupanič Pajnič I. Molecular genetic analyses of 300-year old skeletons from Auersperg tomb [in Slovenian]. Zdrav Vestn. 2013;82:796–808.
Zupanič Pajnič I, Zupanc T, Balažic J, Geršak ŽM, Stojković O, Skadrić I, et al. Prediction of autosomal STR typing success in ancient and Second World War bone samples. Forensic Sci Int Genet. 2017 Mar;27:17–26. https://doi.org/10.1016/j.fsigen.2016.11.004 PMID:27907810
Zupanič Pajnič I, Petaros A, Balažic J, Geršak K. Searching for the mother missed since the Second World War. J Forensic Leg Med. 2016 Nov;44:138–42. https://doi.org/10.1016/j.jflm.2016.10.015 PMID:27810583
Cattaneo C, Craig OE, James NT, Sokol RJ. Comparison of three DNA extraction methods on bone and blood stains up to 43 years old and amplification of three different gene sequences. J Forensic Sci. 1997 Nov;42(6):1126–35. https://doi.org/10.1520/JFS14273J PMID:9397557
Pilli E, Boccone S, Agostino A, Virgili A, D’Errico G, Lari M, et al. From unknown to known: identification of the remains at the mausoleum of fosse Ardeatine. Sci Justice. 2018 Nov;58(6):469–78. https://doi.org/10.1016/j.scijus.2018.05.007 PMID:30446077
Knapp M, Lalueza-Fox C, Hofreiter M. Re-inventing ancient human DNA. Investig Genet. 2015 May;6(1):4. https://doi.org/10.1186/s13323-015-0020-4 PMID:25937886
Mehta B, Daniel R, Phillips C, McNevin D. Forensically relevant SNaPshot® assays for human DNA SNP analysis: a review. Int J Legal Med. 2017 Jan;131(1):21–37. https://doi.org/10.1007/s00414-016-1490-5 PMID:27841004
Balding D. Weight-of-evidence for Forensic DNA Profiles. West Sussex, England: John Wiley & Sons; 2005. pp. 50–1. https://doi.org/10.1002/9780470867693.
Gill P, Ivanov PL, Kimpton C, Piercy R, Benson N, Tully G, et al. Identification of the remains of the Romanov family by DNA analysis. Nat Genet. 1994 Feb;6(2):130–5. https://doi.org/10.1038/ng0294-130 PMID:8162066
Jehaes E, Toprak K, Vanderheyden N, Pfeiffer H, Cassiman JJ, Brinkmann B, et al. Pitfalls in the analysis of mitochondrial DNA from ancient specimens and the consequences for forensic DNA analysis: the historical case of the putative heart of Louis XVII. Int J Legal Med. 2001 Dec;115(3):135–41. https://doi.org/10.1007/s004140100221 PMID:11775015
King TE, Fortes GG, Balaresque P, Thomas MG, Balding D, Maisano Delser P, et al. Identification of the remains of King Richard III. Nat Commun. 2014 Dec;5(1):5631. https://doi.org/10.1038/ncomms6631 PMID:25463651
Kayser M, de Knijff P. Improving human forensics through advances in genetics, genomics and molecular biology. Nat Rev Genet. 2011 Mar;12(3):179–92. https://doi.org/10.1038/nrg2952 PMID:21331090
Walsh S, Liu F, Wollstein A, Kovatsi L, Ralf A, Kosiniak-Kamysz A, et al. The HIrisPlex system for simultaneous prediction of hair and eye colour from DNA. Forensic Sci Int Genet. 2013 Jan;7(1):98–115. https://doi.org/10.1016/j.fsigen.2012.07.005 PMID:22917817
Phillips C, Prieto L, Fondevila M, Salas A, Gómez-Tato A, Alvarez-Dios J, et al. Ancestry analysis in the 11-M Madrid bomb attack investigation. PLoS One. 2009 Aug;4(8):e6583. https://doi.org/10.1371/journal.pone.0006583 PMID:19668368
Karafet TM, Mendez FL, Meilerman MB, Underhill PA, Zegura SL, Hammer MF. New binary polymorphisms reshape and increase resolution of the human Y chromosomal haplogroup tree. Genome Res. 2008 May;18(5):830–8. https://doi.org/10.1101/gr.7172008 PMID:18385274
Larmuseau MH, Vanderheyden N, Van Geystelen A, van Oven M, Kayser M, Decorte R. Increasing phylogenetic resolution still informative for Y chromosomal studies on West-European populations. Forensic Sci Int Genet. 2014 Mar;9:179–85. https://doi.org/10.1016/j.fsigen.2013.04.002 PMID:23683810
Larmuseau MH, Otten GP, Decorte R, Van Damme P, Moisse M. Defining Y-SNP variation among the Flemish population (Western Europe) by full genome sequencing. Forensic Sci Int Genet. 2017 Nov;31:e12–6. https://doi.org/10.1016/j.fsigen.2017.10.008 PMID:29089250
Kosoy R, Nassir R, Tian C, White PA, Butler LM, Silva G, et al. Ancestry informative marker sets for determining continental origin and admixture proportions in common populations in America. Hum Mutat. 2009 Jan;30(1):69–78. https://doi.org/10.1002/humu.20822 PMID:18683858
Espregueira Themudo G, Smidt Mogensen H, Børsting C, Morling N. Frequencies of HID-ion ampliseq ancestry panel markers among greenlanders. Forensic Sci Int Genet. 2016 Sep;24:60–4. https://doi.org/10.1016/j.fsigen.2016.06.001 PMID:27326551
Phillips C, Salas A, Sánchez JJ, Fondevila M, Gómez-Tato A, Alvarez-Dios J, et al.; SNPforID Consortium. Inferring ancestral origin using a single multiplex assay of ancestry-informative marker SNPs. Forensic Sci Int Genet. 2007 Dec;1(3-4):273–80. https://doi.org/10.1016/j.fsigen.2007.06.008 PMID:19083773
Kidd KK, Speed WC, Pakstis AJ, Furtado MR, Fang R, Madbouly A, et al. Progress toward an efficient panel of SNPs for ancestry inference. Forensic Sci Int Genet. 2014 May;10:23–32. https://doi.org/10.1016/j.fsigen.2014.01.002 PMID:24508742
Silvia AL, Shugarts N, Smith J. A preliminary assessment of the ForenSeq™ FGx System: next generation sequencing of an STR and SNP multiplex. Int J Legal Med. 2017 Jan;131(1):73–86. https://doi.org/10.1007/s00414-016-1457-6 PMID:27785563
Fulton LT. Ancient DNA - Methods and Protocols: Setting up an ancient DNA laboratory. NJ: Humana Press Inc; 2012. pp. 1–11.
Lindahl T. Instability and decay of the primary structure of DNA. Nature. 1993 Apr;362(6422):709–15. https://doi.org/10.1038/362709a0 PMID:8469282
Salamon M, Tuross N, Arensburg B, Weiner S. Relatively well preserved DNA is present in the crystal aggregates of fossil bones. Proc Natl Acad Sci USA. 2005 Sep;102(39):13783–8. https://doi.org/10.1073/pnas.0503718102 PMID:16162675
Rohland N, Hofreiter M. Ancient DNA extraction from bones and teeth. Nat Protoc. 2007;2(7):1756–62. https://doi.org/10.1038/nprot.2007.247 PMID:17641642
Graham EA. DNA reviews: ancient DNA. Forensic Sci Med Pathol. 2007 Sep;3(3):221–5. https://doi.org/10.1007/s12024-007-9009-5 PMID:25869168
Jakubowska J, Maciejewska A, Pawłowski R. Comparison of three methods of DNA extraction from human bones with different degrees of degradation. Int J Legal Med. 2012 Jan;126(1):173–8. https://doi.org/10.1007/s00414-011-0590-5 PMID:21717154
Amory S, Huel R, Bilić A, Loreille O, Parsons TJ. Automatable full demineralization DNA extraction procedure from degraded skeletal remains. Forensic Sci Int Genet. 2012 May;6(3):398–406. https://doi.org/10.1016/j.fsigen.2011.08.004 PMID:21885362
Zupanič Pajnič I, Debska M, Gornjak Pogorelc B, Vodopivec Mohorčič K, Balažic J, Zupanc T, et al. Highly efficient automated extraction of DNA from old and contemporary skeletal remains. J Forensic Leg Med. 2016 Jan;37:78–86. https://doi.org/10.1016/j.jflm.2015.11.001 PMID:26615474
Bender K, Schneider PM, Rittner C. Application of mtDNA sequence analysis in forensic casework for the identification of human remains. Forensic Sci Int. 2000 Sep;113(1-3):103–7. https://doi.org/10.1016/S0379-0738(00)00223-1 PMID:10978609
Loreille OM, Diegoli TM, Irwin JA, Coble MD, Parsons TJ. High efficiency DNA extraction from bone by total demineralization. Forensic Sci Int Genet. 2007 Jun;1(2):191–5. https://doi.org/10.1016/j.fsigen.2007.02.006 PMID:19083754
Ewing MM, Thompson JM, McLaren RS, Purpero VM, Thomas KJ, Dobrowski PA, et al. Human DNA quantification and sample quality assessment: developmental validation of the PowerQuant(®) system. Forensic Sci Int Genet. 2016 Jul;23:166–77. https://doi.org/10.1016/j.fsigen.2016.04.007 PMID:27206225
Zupanič Pajnič I. Extraction of DNA from Human Skeletal Material. In: Goodwin W: Forensic DNA Typing Protocols. Methods in Molecular Biology. Humana Press, New York, NY, 2016;1420:89-108.
Zupanič Pajnič I, Gornjak Pogorelc B, Balažic J, Zupanc T, Štefanič B. Highly efficient nuclear DNA typing of the World War II skeletal remains using three new autosomal short tandem repeat amplification kits with the extended European Standard Set of loci. Croat Med J. 2012 Feb;53(1):17–23. https://doi.org/10.3325/cmj.2012.53.17 PMID:22351574
Geršak ŽM. Določitev primernosti drobnih kosti nog in rok za molekularno genetsko tipizacijo starih skeletnih ostankov [fakultetna Prešernova naloga]. Ljubljana: ŽM. Geršak; 2017.
Chaitanya L, Pajnič IZ, Walsh S, Balažic J, Zupanc T, Kayser M. Bringing colour back after 70 years: predicting eye and hair colour from skeletal remains of World War II victims using the HIrisPlex system. Forensic Sci Int Genet. 2017 Jan;26:48–57. https://doi.org/10.1016/j.fsigen.2016.10.004 PMID:27780108
Strobl C, Eduardoff M, Bus MM, Allen M, Parson W. Evaluation of the precision ID whole MtDNA genome panel for forensic analyses. Forensic Sci Int Genet. 2018 Jul;35:21–5. https://doi.org/10.1016/j.fsigen.2018.03.013 PMID:29626805
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