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Home / Equine Research Bank / Mol Ecol Resour / Performance and automation of ancient DNA capture with RNA h...
Molecular ecology resources2021; 22(3); 891-907; doi: 10.1111/1755-0998.13518

Performance and automation of ancient DNA capture with RNA hyRAD probes.

Abstract: DNA hybridization-capture techniques allow researchers to focus their sequencing efforts on preselected genomic regions. This feature is especially useful when analysing ancient DNA (aDNA) extracts, which are often dominated by exogenous environmental sources. Here, we assessed, for the first time, the performance of hyRAD as an inexpensive and design-free alternative to commercial capture protocols to obtain authentic aDNA data from osseous remains. HyRAD relies on double enzymatic restriction of fresh DNA extracts to produce RNA probes that cover only a fraction of the genome and can serve as baits for capturing homologous fragments from aDNA libraries. We found that this approach could retrieve sequence data from horse remains coming from a range of preservation environments, including beyond radiocarbon range, yielding up to 146.5-fold on-target enrichment for aDNA extracts showing extremely low endogenous content (20%-30%), while the fraction of endogenous reads mapping on- and off-target was relatively insensitive to the original endogenous DNA content. Procedures based on two instead of a single round of capture increased on-target coverage up to 3.6-fold. Additionally, we used methylation-sensitive restriction enzymes to produce probes targeting hypomethylated regions, which improved data quality by reducing post-mortem DNA damage and mapping within multicopy regions. Finally, we developed a fully automated hyRAD protocol utilizing inexpensive robotic platforms to facilitate capture processing. Overall, our work establishes hyRAD as a cost-effective strategy to recover a set of shared orthologous variants across multiple ancient samples.
© 2021 The Authors. Molecular Ecology Resources published by John Wiley & Sons Ltd.
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Publication Date: 2021-10-15 PubMed ID: 34582623PubMed Central: PMC9291508DOI: 10.1111/1755-0998.13518Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The study presents the first evaluation of hyRAD, an economical and easily customizable alternative to standard commercial protocols, to extract ancient DNA data from bone remains. The research confirms hyRAD’s effectiveness in retrieving sequence data from horse remains originating across different preservation environments, making it a cost-effective tool for capturing shared genetic variants across multiple ancient samples.

Underlying Concept

  • HyRAD is described as an inexpensive alternative to standard commercial protocols for capturing specific genomic regions in ancient DNA analyses, which are typically populated by foreign environmental elements.
  • The method uses double enzymatic restriction processes on fresh DNA extracts to produce RNA probes, which only target a fraction of the genome. These probes act as baits in capturing matching fragments in ancient DNA libraries.

Evaluation and Performance

  • The evaluation was carried out using horse remains from various preservation environments, including some that are beyond the capacity of radiocarbon dating methods.
  • The on-target enrichment achieved was up to 146.5-fold for ancient DNA extracts with very low inherent content (<1%).
  • For samples with good DNA preservation (>20%-30%), however, the performance was less significant.
  • Interestingly, the fraction of endogenous reads mapping on- and off-target was not greatly affected by the initial endogenous DNA content.
  • Procedures that employs two capture rounds instead of just one enhanced on-target coverage by up to 3.6 times.

Improvements and Innovations

  • The researchers also used methylation-sensitive restriction enzymes to create probes that target hypomethylated regions, thus improving data quality by reducing post-mortem DNA damage and sequence mapping within multicopy regions.
  • An entirely automated hyRAD protocol was developed which utilizes economical robotic platforms to enable easier capture processing.

Conclusion

  • Overall, the research validates hyRAD as a cost-effective strategy for recovering shared orthologous variants across multiple ancient samples.

Cite This Article

APA
Suchan T, Kusliy MA, Khan N, Chauvey L, Tonasso-Calvière L, Schiavinato S, Southon J, Keller M, Kitagawa K, Krause J, Bessudnov AN, Bessudnov AA, Graphodatsky AS, Valenzuela-Lamas S, Wilczyński J, Pospuła S, Tunia K, Nowak M, Moskal-delHoyo M, Tishkin AA, Pryor AJE, Outram AK, Orlando L. (2021). Performance and automation of ancient DNA capture with RNA hyRAD probes. Mol Ecol Resour, 22(3), 891-907. https://doi.org/10.1111/1755-0998.13518

Publication

Molecular ecology resources
ISSN: 1755-0998
NlmUniqueID: 101465604
Country: England
Language: English
Volume: 22
Issue: 3
Pages: 891-907

Researcher Affiliations

Suchan, Tomasz
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
Kusliy, Mariya A
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
  • Department of the Diversity and Evolution of Genomes, Institute of Molecular and Cellular Biology SB RAS, Novosibirsk, Russia.
Khan, Naveed
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
  • Department of Biotechnology, Abdul Wali Khan University, Mardan, Pakistan.
Chauvey, Loreleï
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
Tonasso-Calvière, Laure
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
Schiavinato, Stéphanie
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.
Southon, John
  • Earth System Science Department, University of California, Irvine, Irvine, California, USA.
Keller, Marcel
  • Estonian Biocentre, Institute of Genomics, University of Tartu, Tartu, Estonia.
Kitagawa, Keiko
  • SFB 1070 ResourceCultures, University of Tübingen, Tübingen, Germany.
  • Department of Early Prehistory and Quaternary Ecology, University of Tübingen, Tübingen, Germany.
Krause, Johannes
  • Department of Archaeogenetics, Max Planck Institute for the Science of Human History, Jena, Germany.
  • Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Bessudnov, Alexander N
  • Lipetsk State Pedagogical P. Semyonov-Tyan-Shansky University, Lipetsk, Russia.
Bessudnov, Alexander A
  • Institute for the History of Material Culture, Russian Academy of Sciences, Saint Petersburg, Russia.
Graphodatsky, Alexander S
  • Department of the Diversity and Evolution of Genomes, Institute of Molecular and Cellular Biology SB RAS, Novosibirsk, Russia.
Valenzuela-Lamas, Silvia
  • Institución Milà i Fontanals de Humanidades, Consejo Superior de Investigaciones Científicas (IMF-CSIC), Barcelona, Spain.
Wilczyński, Jarosław
  • Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland.
Pospuła, Sylwia
  • Institute of Systematics and Evolution of Animals, Polish Academy of Sciences, Kraków, Poland.
Tunia, Krzysztof
  • Institute of Archaeology and Ethnology, Polish Academy of Sciences, Kraków, Poland.
Nowak, Marek
  • Institute of Archaeology, Jagiellonian University, Kraków, Poland.
Moskal-delHoyo, Magdalena
  • W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków, Poland.
Tishkin, Alexey A
  • Department of Archaeology, Ethnography and Museology, Altai State University, Barnaul, Russia.
Pryor, Alexander J E
  • Department of Archaeology, University of Exeter, Exeter, UK.
Outram, Alan K
  • Department of Archaeology, University of Exeter, Exeter, UK.
Orlando, Ludovic
  • Centre d'Anthropobiologie et de Génomique de Toulouse (CAGT), Université Paul Sabatier, Faculté de Médecine Purpan, Toulouse, France.

MeSH Terms

  • Animals
  • Automation
  • DNA, Ancient
  • Horses / genetics
  • RNA / genetics
  • RNA Probes
  • Sequence Analysis, DNA / methods

Grant Funding

  • CNRS International Research Project (IRP AMADEUS)
  • CNRS Programme de Recherche Conjoint (PRC)
  • 681605 / H2020 European Research Council
  • 797449 / H2020 Marie Sku0142odowska-Curie Actions
  • 19-59-15001 / Russian Foundation for Basic Research
  • University Paul Sabatier IDEX Chaire d'Excellence (OURASI)

References

This article includes 67 references
  1. Aylward ML, Sullivan AP, Perry GH, Johnson SE, Louis EE Jr. An environmental DNA sampling method for aye-ayes from their feeding traces.. Ecol Evol 2018 Sep;8(18):9229-9240.
    doi: 10.1002/ece3.4341pmc: PMC6194247pubmed: 30377496google scholar: lookup
  2. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA. Rapid SNP discovery and genetic mapping using sequenced RAD markers.. PLoS One 2008;3(10):e3376.
    doi: 10.1371/journal.pone.0003376pmc: PMC2557064pubmed: 18852878google scholar: lookup
  3. Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed‐effects models using lme4. Journal of Statistical Software 67(1), 1–48.
    doi: 10.18637/jss.v067.i01google scholar: lookup
  4. Boucher FC, Casazza G, Szövényi P, Conti E. Sequence capture using RAD probes clarifies phylogenetic relationships and species boundaries in Primula sect. Auricula.. Mol Phylogenet Evol 2016 Nov;104:60-72.
    doi: 10.1016/j.ympev.2016.08.003pubmed: 27502126google scholar: lookup
  5. Briggs AW, Stenzel U, Johnson PL, Green RE, Kelso J, Prüfer K, Meyer M, Krause J, Ronan MT, Lachmann M, Pääbo S. Patterns of damage in genomic DNA sequences from a Neandertal.. Proc Natl Acad Sci U S A 2007 Sep 11;104(37):14616-21.
    doi: 10.1073/pnas.0704665104pmc: PMC1976210pubmed: 17715061google scholar: lookup
  6. Cahill JA, Heintzman PD, Harris K, Teasdale MD, Kapp J, Soares AER, Stirling I, Bradley D, Edwards CJ, Graim K, Kisleika AA, Malev AV, Monaghan N, Green RE, Shapiro B. Genomic Evidence of Widespread Admixture from Polar Bears into Brown Bears during the Last Ice Age.. Mol Biol Evol 2018 May 1;35(5):1120-1129.
    doi: 10.1093/molbev/msy018pubmed: 29471451google scholar: lookup
  7. Carpenter ML, Buenrostro JD, Valdiosera C, Schroeder H, Allentoft ME, Sikora M, Rasmussen M, Gravel S, Guillén S, Nekhrizov G, Leshtakov K, Dimitrova D, Theodossiev N, Pettener D, Luiselli D, Sandoval K, Moreno-Estrada A, Li Y, Wang J, Gilbert MT, Willerslev E, Greenleaf WJ, Bustamante CD. Pulling out the 1%: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries.. Am J Hum Genet 2013 Nov 7;93(5):852-64.
    doi: 10.1016/j.ajhg.2013.10.002pmc: PMC3824117pubmed: 24568772google scholar: lookup
  8. Chafin TK, Martin BT, Mussmann SM, Douglas MR, Douglas ME. FRAGMATIC: In silico locus prediction and its utility in optimizing ddRADseq projects. Conservation Genetics Resources 10(3), 325–328.
    doi: 10.1007/s12686-017-0814-1google scholar: lookup
  9. Crates R, Olah G, Adamski M, Aitken N, Banks S, Ingwersen D, Ranjard L, Rayner L, Stojanovic D, Suchan T, von Takach Dukai B, Heinsohn R. Genomic impact of severe population decline in a nomadic songbird.. PLoS One 2019;14(10):e0223953.
    doi: 10.1371/journal.pone.0223953pmc: PMC6812763pubmed: 31647830google scholar: lookup
  10. Cruz-Dávalos DI, Llamas B, Gaunitz C, Fages A, Gamba C, Soubrier J, Librado P, Seguin-Orlando A, Pruvost M, Alfarhan AH, Alquraishi SA, Al-Rasheid KAS, Scheu A, Beneke N, Ludwig A, Cooper A, Willerslev E, Orlando L. Experimental conditions improving in-solution target enrichment for ancient DNA.. Mol Ecol Resour 2017 May;17(3):508-522.
    doi: 10.1111/1755-0998.12595pubmed: 27566552google scholar: lookup
  11. Dabney J, Meyer M, Pääbo S. Ancient DNA damage.. Cold Spring Harb Perspect Biol 2013 Jul 1;5(7).
    doi: 10.1101/cshperspect.a012567pmc: PMC3685887pubmed: 23729639google scholar: lookup
  12. Daley T, Smith AD. Predicting the molecular complexity of sequencing libraries.. Nat Methods 2013 Apr;10(4):325-7.
    doi: 10.1038/nmeth.2375pmc: PMC3612374pubmed: 23435259google scholar: lookup
  13. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R. The variant call format and VCFtools.. Bioinformatics 2011 Aug 1;27(15):2156-8.
    doi: 10.1093/bioinformatics/btr330pmc: PMC3137218pubmed: 21653522google scholar: lookup
  14. Enk JM, Devault AM, Kuch M, Murgha YE, Rouillard JM, Poinar HN. Ancient whole genome enrichment using baits built from modern DNA.. Mol Biol Evol 2014 May;31(5):1292-4.
    doi: 10.1093/molbev/msu074pubmed: 24531081google scholar: lookup
  15. Fages A, Hanghøj K, Khan N, Gaunitz C, Seguin-Orlando A, Leonardi M, McCrory Constantz C, Gamba C, Al-Rasheid KAS, Albizuri S, Alfarhan AH, Allentoft M, Alquraishi S, Anthony D, Baimukhanov N, Barrett JH, Bayarsaikhan J, Benecke N, Bernáldez-Sánchez E, Berrocal-Rangel L, Biglari F, Boessenkool S, Boldgiv B, Brem G, Brown D, Burger J, Crubézy E, Daugnora L, Davoudi H, de Barros Damgaard P, de Los Ángeles de Chorro Y de Villa-Ceballos M, Deschler-Erb S, Detry C, Dill N, do Mar Oom M, Dohr A, Ellingvåg S, Erdenebaatar D, Fathi H, Felkel S, Fernández-Rodríguez C, García-Viñas E, Germonpré M, Granado JD, Hallsson JH, Hemmer H, Hofreiter M, Kasparov A, Khasanov M, Khazaeli R, Kosintsev P, Kristiansen K, Kubatbek T, Kuderna L, Kuznetsov P, Laleh H, Leonard JA, Lhuillier J, Liesau von Lettow-Vorbeck C, Logvin A, Lõugas L, Ludwig A, Luis C, Arruda AM, Marques-Bonet T, Matoso Silva R, Merz V, Mijiddorj E, Miller BK, Monchalov O, Mohaseb FA, Morales A, Nieto-Espinet A, Nistelberger H, Onar V, Pálsdóttir AH, Pitulko V, Pitskhelauri K, Pruvost M, Rajic Sikanjic P, Rapan Papeša A, Roslyakova N, Sardari A, Sauer E, Schafberg R, Scheu A, Schibler J, Schlumbaum A, Serrand N, Serres-Armero A, Shapiro B, Sheikhi Seno S, Shevnina I, Shidrang S, Southon J, Star B, Sykes N, Taheri K, Taylor W, Teegen WR, Trbojević Vukičević T, Trixl S, Tumen D, Undrakhbold S, Usmanova E, Vahdati A, Valenzuela-Lamas S, Viegas C, Wallner B, Weinstock J, Zaibert V, Clavel B, Lepetz S, Mashkour M, Helgason A, Stefánsson K, Barrey E, Willerslev E, Outram AK, Librado P, Orlando L. Tracking Five Millennia of Horse Management with Extensive Ancient Genome Time Series.. Cell 2019 May 30;177(6):1419-1435.e31.
    doi: 10.1016/j.cell.2019.03.049pmc: PMC6547883pubmed: 31056281google scholar: lookup
  16. Fontsere C, Alvarez-Estape M, Lester J, Arandjelovic M, Kuhlwilm M, Dieguez P, Agbor A, Angedakin S, Ayuk Ayimisin E, Bessone M, Brazzola G, Deschner T, Eno-Nku M, Granjon AC, Head J, Kadam P, Kalan AK, Kambi M, Langergraber K, Lapuente J, Maretti G, Jayne Ormsby L, Piel A, Robbins MM, Stewart F, Vergnes V, Wittig RM, Kühl HS, Marques-Bonet T, Hughes DA, Lizano E. Maximizing the acquisition of unique reads in noninvasive capture sequencing experiments.. Mol Ecol Resour 2021 Apr;21(3):745-761.
    doi: 10.1111/1755-0998.13300pubmed: 33217149google scholar: lookup
  17. Furtwängler A, Neukamm J, Böhme L, Reiter E, Vollstedt M, Arora N, Singh P, Cole ST, Knauf S, Calvignac-Spencer S, Krause-Kyora B, Krause J, Schuenemann VJ, Herbig A. Comparison of target enrichment strategies for ancient pathogen DNA.. Biotechniques 2020 Dec;69(6):455-459.
    doi: 10.2144/btn-2020-0100pubmed: 33135465google scholar: lookup
  18. Gamba C, Hanghøj K, Gaunitz C, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, Bradley DG, Orlando L. Comparing the performance of three ancient DNA extraction methods for high-throughput sequencing.. Mol Ecol Resour 2016 Mar;16(2):459-69.
    doi: 10.1111/1755-0998.12470pubmed: 26401836google scholar: lookup
  19. Garrison E, Marth G. Haplotype‐based variant detection from short‐read sequencing. ArXiv 1207.3907 [q‐Bio].
  20. Gauthier J, Pajkovic M, Neuenschwander S, Kaila L, Schmid S, Orlando L, Alvarez N. Museomics identifies genetic erosion in two butterfly species across the 20th century in Finland.. Mol Ecol Resour 2020 Sep;20(5):1191-1205.
    doi: 10.1111/1755-0998.13167pmc: PMC7540272pubmed: 32304133google scholar: lookup
  21. Giguet-Covex C, Pansu J, Arnaud F, Rey PJ, Griggo C, Gielly L, Domaizon I, Coissac E, David F, Choler P, Poulenard J, Taberlet P. Long livestock farming history and human landscape shaping revealed by lake sediment DNA.. Nat Commun 2014;5:3211.
    doi: 10.1038/ncomms4211pubmed: 24487920google scholar: lookup
  22. Goodwin S, McPherson JD, McCombie WR. Coming of age: ten years of next-generation sequencing technologies.. Nat Rev Genet 2016 May 17;17(6):333-51.
    doi: 10.1038/nrg.2016.49pubmed: 27184599google scholar: lookup
  23. Hanghøj K, Seguin-Orlando A, Schubert M, Madsen T, Pedersen JS, Willerslev E, Orlando L. Fast, Accurate and Automatic Ancient Nucleosome and Methylation Maps with epiPALEOMIX.. Mol Biol Evol 2016 Dec;33(12):3284-3298.
    doi: 10.1093/molbev/msw184pmc: PMC5100044pubmed: 27624717google scholar: lookup
  24. Hernandez-Rodriguez J, Arandjelovic M, Lester J, de Filippo C, Weihmann A, Meyer M, Angedakin S, Casals F, Navarro A, Vigilant L, Kühl HS, Langergraber K, Boesch C, Hughes D, Marques-Bonet T. The impact of endogenous content, replicates and pooling on genome capture from faecal samples.. Mol Ecol Resour 2018 Mar;18(2):319-333.
    doi: 10.1111/1755-0998.12728pmc: PMC5900898pubmed: 29058768google scholar: lookup
  25. Holland I, Davies JA. Automation in the Life Science Research Laboratory.. Front Bioeng Biotechnol 2020;8:571777.
    doi: 10.3389/fbioe.2020.571777pmc: PMC7691657pubmed: 33282848google scholar: lookup
  26. Jónsson H, Ginolhac A, Schubert M, Johnson PL, Orlando L. mapDamage2.0: fast approximate Bayesian estimates of ancient DNA damage parameters.. Bioinformatics 2013 Jul 1;29(13):1682-4.
    doi: 10.1093/bioinformatics/btt193pmc: PMC3694634pubmed: 23613487google scholar: lookup
  27. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  28. Karam MJ, Lefèvre F, Dagher-Kharrat MB, Pinosio S, Vendramin GG. Genomic exploration and molecular marker development in a large and complex conifer genome using RADseq and mRNAseq.. Mol Ecol Resour 2015 May;15(3):601-12.
    doi: 10.1111/1755-0998.12329pubmed: 25224750google scholar: lookup
  29. Kozarewa I, Armisen J, Gardner AF, Slatko BE, Hendrickson CL. Overview of Target Enrichment Strategies.. Curr Protoc Mol Biol 2015 Oct 1;112:7.21.1-7.21.23.
    doi: 10.1002/0471142727.mb0721s112pubmed: 26423591google scholar: lookup
  30. Lang PLM, Weiß CL, Kersten S, Latorre SM, Nagel S, Nickel B, Meyer M, Burbano HA. Hybridization ddRAD-sequencing for population genomics of nonmodel plants using highly degraded historical specimen DNA.. Mol Ecol Resour 2020 Sep;20(5):1228-1247.
    doi: 10.1111/1755-0998.13168pubmed: 32306514google scholar: lookup
  31. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2.. Nat Methods 2012 Mar 4;9(4):357-9.
    doi: 10.1038/nmeth.1923pmc: PMC3322381pubmed: 22388286google scholar: lookup
  32. Larsson H, De Paoli E, Morgante M, Lascoux M, Gyllenstrand N. The Hypomethylated Partial Restriction (HMPR) method reduces the repetitive content of genomic libraries in Norway spruce (Picea abies). Tree Genetics & Genomes 9(2), 601–612.
    doi: 10.1007/s11295-012-0582-8google scholar: lookup
  33. Leonardi M, Librado P, Der Sarkissian C, Schubert M, Alfarhan AH, Alquraishi SA, Al-Rasheid KA, Gamba C, Willerslev E, Orlando L. Evolutionary Patterns and Processes: Lessons from Ancient DNA.. Syst Biol 2017 Jan 1;66(1):e1-e29.
    doi: 10.1093/sysbio/syw059pmc: PMC5410953pubmed: 28173586google scholar: lookup
  34. Lesnik EA, Freier SM. Relative thermodynamic stability of DNA, RNA, and DNA:RNA hybrid duplexes: relationship with base composition and structure.. Biochemistry 1995 Aug 29;34(34):10807-15.
    doi: 10.1021/bi00034a013pubmed: 7662660google scholar: lookup
  35. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools.. Bioinformatics 2009 Aug 15;25(16):2078-9.
    doi: 10.1093/bioinformatics/btp352pmc: PMC2723002pubmed: 19505943google scholar: lookup
  36. Linck EB, Hanna ZR, Sellas A, Dumbacher JP. Evaluating hybridization capture with RAD probes as a tool for museum genomics with historical bird specimens.. Ecol Evol 2017 Jul;7(13):4755-4767.
    doi: 10.1002/ece3.3065pmc: PMC5496524pubmed: 28690805google scholar: lookup
  37. Mamanova L, Coffey AJ, Scott CE, Kozarewa I, Turner EH, Kumar A, Howard E, Shendure J, Turner DJ. Target-enrichment strategies for next-generation sequencing.. Nat Methods 2010 Feb;7(2):111-8.
    doi: 10.1038/nmeth.1419pubmed: 20111037google scholar: lookup
  38. Maricic T, Whitten M, Pääbo S. Multiplexed DNA sequence capture of mitochondrial genomes using PCR products.. PLoS One 2010 Nov 16;5(11):e14004.
    doi: 10.1371/journal.pone.0014004pmc: PMC2982832pubmed: 21103372google scholar: lookup
  39. Martin M. Cutadapt removes adapter sequences from high‐throughput sequencing reads. EMBnet.Journal 17(1), 10.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  40. Mathieson I, Lazaridis I, Rohland N, Mallick S, Patterson N, Roodenberg SA, Harney E, Stewardson K, Fernandes D, Novak M, Sirak K, Gamba C, Jones ER, Llamas B, Dryomov S, Pickrell J, Arsuaga JL, de Castro JM, Carbonell E, Gerritsen F, Khokhlov A, Kuznetsov P, Lozano M, Meller H, Mochalov O, Moiseyev V, Guerra MA, Roodenberg J, Vergès JM, Krause J, Cooper A, Alt KW, Brown D, Anthony D, Lalueza-Fox C, Haak W, Pinhasi R, Reich D. Genome-wide patterns of selection in 230 ancient Eurasians.. Nature 2015 Dec 24;528(7583):499-503.
    doi: 10.1038/nature16152pmc: PMC4918750pubmed: 26595274google scholar: lookup
  41. May M. A DIY approach to automating your lab.. Nature 2019 May;569(7757):587-588.
    doi: 10.1038/d41586-019-01590-zpubmed: 31110319google scholar: lookup
  42. McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT. Applications of next-generation sequencing to phylogeography and phylogenetics.. Mol Phylogenet Evol 2013 Feb;66(2):526-38.
    doi: 10.1016/j.ympev.2011.12.007pubmed: 22197804google scholar: lookup
  43. Meyer M, Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing.. Cold Spring Harb Protoc 2010 Jun;2010(6):pdb.prot5448.
    doi: 10.1101/pdb.prot5448pubmed: 20516186google scholar: lookup
  44. Orlando L. The Evolutionary and Historical Foundation of the Modern Horse: Lessons from Ancient Genomics.. Annu Rev Genet 2020 Nov 23;54:563-581.
    doi: 10.1146/annurev-genet-021920-011805pubmed: 32960653google scholar: lookup
  45. Orlando L, Cooper A. Using Ancient DNA to Understand Evolutionary and Ecological Processes. Annual Review of Ecology, Evolution, and Systematics 45(1), 573–598.
    doi: 10.1146/annurev-ecolsys-120213-091712google scholar: lookup
  46. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    doi: 10.1038/nature12323pubmed: 23803765google scholar: lookup
  47. Pedersen MW, Ruter A, Schweger C, Friebe H, Staff RA, Kjeldsen KK, Mendoza ML, Beaudoin AB, Zutter C, Larsen NK, Potter BA, Nielsen R, Rainville RA, Orlando L, Meltzer DJ, Kjær KH, Willerslev E. Postglacial viability and colonization in North America's ice-free corridor.. Nature 2016 Sep 1;537(7618):45-49.
    doi: 10.1038/nature19085pubmed: 27509852google scholar: lookup
  48. Peñalba JV, Smith LL, Tonione MA, Sass C, Hykin SM, Skipwith PL, McGuire JA, Bowie RC, Moritz C. Sequence capture using PCR-generated probes: a cost-effective method of targeted high-throughput sequencing for nonmodel organisms.. Mol Ecol Resour 2014 Sep;14(5):1000-10.
    doi: 10.1111/1755-0998.12249pubmed: 24618181google scholar: lookup
  49. Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE. Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species.. PLoS One 2012;7(5):e37135.
    doi: 10.1371/journal.pone.0037135pmc: PMC3365034pubmed: 22675423google scholar: lookup
  50. Poullet M, Orlando L. Assessing DNA Sequence Alignment Methods for Characterizing Ancient Genomes and Methylomes. Frontiers in Ecology and Evolution 8, 105.
    doi: 10.3389/fevo.2020.00105google scholar: lookup
  51. Prüfer K, Stenzel U, Hofreiter M, Pääbo S, Kelso J, Green RE. Computational challenges in the analysis of ancient DNA.. Genome Biol 2010;11(5):R47.
    doi: 10.1186/gb-2010-11-5-r47pmc: PMC2898072pubmed: 20441577google scholar: lookup
  52. Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features.. Bioinformatics 2010 Mar 15;26(6):841-2.
    doi: 10.1093/bioinformatics/btq033pmc: PMC2832824pubmed: 20110278google scholar: lookup
  53. R Core Team. R: A Language and Environment for Statistical Computing. .
  54. Rohland N, Harney E, Mallick S, Nordenfelt S, Reich D. Partial uracil-DNA-glycosylase treatment for screening of ancient DNA.. Philos Trans R Soc Lond B Biol Sci 2015 Jan 19;370(1660):20130624.
    doi: 10.1098/rstb.2013.0624pmc: PMC4275898pubmed: 25487342google scholar: lookup
  55. Schmid S, Genevest R, Gobet E, Suchan T, Sperisen C, Tinner W, Alvarez N. HyRAD‐X, a versatile method combining exome capture and RAD sequencing to extract genomic information from ancient DNA. Methods in Ecology and Evolution 8(10), 1374–1388.
    doi: 10.1111/2041-210X.12785google scholar: lookup
  56. Schmid S, Neuenschwander S, Pitteloud C, Heckel G, Pajkovic M, Arlettaz R, Alvarez N. Spatial and temporal genetic dynamics of the grasshopper Oedaleus decorus revealed by museum genomics.. Ecol Evol 2018 Feb;8(3):1480-1495.
    doi: 10.1002/ece3.3699pmc: PMC5792620pubmed: 29435226google scholar: lookup
  57. Schubert M, Ermini L, Der Sarkissian C, Jónsson H, Ginolhac A, Schaefer R, Martin MD, Fernández R, Kircher M, McCue M, Willerslev E, Orlando L. Characterization of ancient and modern genomes by SNP detection and phylogenomic and metagenomic analysis using PALEOMIX.. Nat Protoc 2014 May;9(5):1056-82.
    doi: 10.1038/nprot.2014.063pubmed: 24722405google scholar: lookup
  58. Schubert M, Lindgreen S, Orlando L. AdapterRemoval v2: rapid adapter trimming, identification, and read merging.. BMC Res Notes 2016 Feb 12;9:88.
    doi: 10.1186/s13104-016-1900-2pmc: PMC4751634pubmed: 26868221google scholar: lookup
  59. Seguin-Orlando A, Gamba C, Sarkissian C, Ermini L, Louvel G, Boulygina E, Sokolov A, Nedoluzhko A, Lorenzen ED, Lopez P, McDonald HG, Scott E, Tikhonov A, Stafford TW Jr, Alfarhan AH, Alquraishi SA, Al-Rasheid KAS, Shapiro B, Willerslev E, Prokhortchouk E, Orlando L. Pros and cons of methylation-based enrichment methods for ancient DNA.. Sci Rep 2015 Jul 2;5:11826.
    doi: 10.1038/srep11826pmc: PMC4488743pubmed: 26134828google scholar: lookup
  60. Skoglund P, Northoff BH, Shunkov MV, Derevianko AP, Pääbo S, Krause J, Jakobsson M. Separating endogenous ancient DNA from modern day contamination in a Siberian Neandertal.. Proc Natl Acad Sci U S A 2014 Feb 11;111(6):2229-34.
    doi: 10.1073/pnas.1318934111pmc: PMC3926038pubmed: 24469802google scholar: lookup
  61. Slon V, Hopfe C, Weiß CL, Mafessoni F, de la Rasilla M, Lalueza-Fox C, Rosas A, Soressi M, Knul MV, Miller R, Stewart JR, Derevianko AP, Jacobs Z, Li B, Roberts RG, Shunkov MV, de Lumley H, Perrenoud C, Gušić I, Kućan Ž, Rudan P, Aximu-Petri A, Essel E, Nagel S, Nickel B, Schmidt A, Prüfer K, Kelso J, Burbano HA, Pääbo S, Meyer M. Neandertal and Denisovan DNA from Pleistocene sediments.. Science 2017 May 12;356(6338):605-608.
    doi: 10.1126/science.aam9695pubmed: 28450384google scholar: lookup
  62. Smith O, Clapham AJ, Rose P, Liu Y, Wang J, Allaby RG. Genomic methylation patterns in archaeological barley show de-methylation as a time-dependent diagenetic process.. Sci Rep 2014 Jul 4;4:5559.
    doi: 10.1038/srep05559pmc: PMC4081896pubmed: 24993353google scholar: lookup
  63. Suchan T, Pitteloud C, Gerasimova NS, Kostikova A, Schmid S, Arrigo N, Pajkovic M, Ronikier M, Alvarez N. Hybridization Capture Using RAD Probes (hyRAD), a New Tool for Performing Genomic Analyses on Collection Specimens.. PLoS One 2016;11(3):e0151651.
    doi: 10.1371/journal.pone.0151651pmc: PMC4801390pubmed: 26999359google scholar: lookup
  64. Toussaint EFA, Gauthier J, Bilat J, Gillett CPDT, Gough HM, Lundkvist H, Blanc M, Muñoz-Ramírez CP, Alvarez N. HyRAD-X Exome Capture Museomics Unravels Giant Ground Beetle Evolution.. Genome Biol Evol 2021 Jul 6;13(7).
    doi: 10.1093/gbe/evab112pmc: PMC8480185pubmed: 33988685google scholar: lookup
  65. van der Valk T, Pečnerová P, Díez-Del-Molino D, Bergström A, Oppenheimer J, Hartmann S, Xenikoudakis G, Thomas JA, Dehasque M, Sağlıcan E, Fidan FR, Barnes I, Liu S, Somel M, Heintzman PD, Nikolskiy P, Shapiro B, Skoglund P, Hofreiter M, Lister AM, Götherström A, Dalén L. Million-year-old DNA sheds light on the genomic history of mammoths.. Nature 2021 Mar;591(7849):265-269.
    doi: 10.1038/s41586-021-03224-9pmc: PMC7116897pubmed: 33597750google scholar: lookup
  66. Wilcox TM, Zarn KE, Piggott MP, Young MK, McKelvey KS, Schwartz MK. Capture enrichment of aquatic environmental DNA: A first proof of concept.. Mol Ecol Resour 2018 Nov;18(6):1392-1401.
    doi: 10.1111/1755-0998.12928pubmed: 30009542google scholar: lookup
  67. Willerslev E, Davison J, Moora M, Zobel M, Coissac E, Edwards ME, Lorenzen ED, Vestergård M, Gussarova G, Haile J, Craine J, Gielly L, Boessenkool S, Epp LS, Pearman PB, Cheddadi R, Murray D, Bråthen KA, Yoccoz N, Binney H, Cruaud C, Wincker P, Goslar T, Alsos IG, Bellemain E, Brysting AK, Elven R, Sønstebø JH, Murton J, Sher A, Rasmussen M, Rønn R, Mourier T, Cooper A, Austin J, Möller P, Froese D, Zazula G, Pompanon F, Rioux D, Niderkorn V, Tikhonov A, Savvinov G, Roberts RG, MacPhee RD, Gilbert MT, Kjær KH, Orlando L, Brochmann C, Taberlet P. Fifty thousand years of Arctic vegetation and megafaunal diet.. Nature 2014 Feb 6;506(7486):47-51.
    doi: 10.1038/nature12921pubmed: 24499916google scholar: lookup

Citations

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  1. Todd ET, Fromentier A, Sutcliffe R, Running Horse Collin Y, Perdereau A, Aury JM, Èche C, Bouchez O, Donnadieu C, Wincker P, Kalbfleisch T, Petersen JL, Orlando L. Imputed genomes of historical horses provide insights into modern breeding.. iScience 2023 Jul 21;26(7):107104.
    doi: 10.1016/j.isci.2023.107104pubmed: 37416458google scholar: lookup
  2. Clavel P, Louis L, Sarkissian C, Thèves C, Gillet C, Chauvey L, Tressières G, Schiavinato S, Calvière-Tonasso L, Telmon N, Clavel B, Jonvel R, Tzortzis S, Bouniol L, Fémolant JM, Klunk J, Poinar H, Signoli M, Costedoat C, Spyrou MA, Seguin-Orlando A, Orlando L. Improving the extraction of ancient Yersinia pestis genomes from the dental pulp.. iScience 2023 May 19;26(5):106787.
    doi: 10.1016/j.isci.2023.106787pubmed: 37250315google scholar: lookup
  3. Zavala EI, Thomas JT, Sturk-Andreaggi K, Daniels-Higginbotham J, Meyers KK, Barrit-Ross S, Aximu-Petri A, Richter J, Nickel B, Berg GE, McMahon TP, Meyer M, Marshall C. Ancient DNA Methods Improve Forensic DNA Profiling of Korean War and World War II Unknowns.. Genes (Basel) 2022 Jan 11;13(1).
    doi: 10.3390/genes13010129pubmed: 35052469google scholar: lookup
  4. Der Sarkissian C, Velsko IM, Fotakis AK, Vågene ÅJ, Hübner A, Fellows Yates JA. Ancient Metagenomic Studies: Considerations for the Wider Scientific Community.. mSystems 2021 Dec 21;6(6):e0131521.
    doi: 10.1128/msystems.01315-21pubmed: 34931883google scholar: lookup
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