Skip to main content

Ancient DNA: Results and prospects (The 30th anniversary)

Abstract

Evolutionary genetics has reached a new level of research thanks to the opportunity to study the genomes of not only present-day but also of ancient organisms. The obtaining of reliable data when working with ancient DNA is possible only in the case of interdisciplinary collaboration between archaeologists, paleontologists, molecular geneticists, and bioinformaticians. Despite laborious and high-cost technologies, the results never cease to amaze and can not only fill the gaps in the knowledge of the evolutionary history of different species but can also review the existing ideas on population development and dynamics. In this review, we discuss the history of the development of investigative techniques in ancient DNA research and the most striking results of these studies, including the most recent achievements.

References

  1. Higuchi, R., Genetic study on the congenital dislocation of the hip, Bull. Tokyo Med. Dent. Univ., 1984, vol. 31, no. 4, pp. 195–207.

    CAS  PubMed  Google Scholar 

  2. Pääbo, S., Molecular cloning of Ancient Egyptian mummy DNA, Nature, 1985, vol. 314, no. 6012, pp. 644–645.

    PubMed  Google Scholar 

  3. Pääbo, S., Kampe, O., Severinsson, L., et al., The association between class-I transplantation antigens and an adenovirus membrane protein, Prog. Allergy, 1985, vol. 36, pp. 114–134.

    PubMed  Google Scholar 

  4. Pääbo, S., Molecular genetic investigations of ancient human remains, Cold Spring. Harb. Symp. Quant. Biol., 1986, vol. 51, pp. 441–446.

    PubMed  Google Scholar 

  5. Mullis, K.B. and Faloona, F.A., Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction, Methods Enzymol., 1987, vol. 155, pp. 335–350.

    CAS  PubMed  Google Scholar 

  6. Pääbo, S., Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification, Proc. Natl. Acad. Sci. U.S.A., 1989, vol. 86, no. 6, pp. 1939–1943.

    PubMed Central  PubMed  Google Scholar 

  7. Golenberg, E.M., Giannasi, D.E., Clegg, M.T., et al., Chloroplast DNA sequence from a Miocene Magnolia species, Nature, 1990, vol. 344, no. 6267, pp. 656–658.

    CAS  PubMed  Google Scholar 

  8. Soltis, P.S.S.D. and Smiley, C.J., An rbcL sequence from a Miocene Taxodium (bald cypress), Proc. Natl. Acad. Sci. U.S.A., 1992, vol. 89, pp. 449–451.

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Willerslev, E., Hansen, A.J., and Poinar, H.N., Isolation of nucleic acids and cultures from fossil ice and permafrost, Trends Ecol. Evol., 2004, vol. 19, no. 3, pp. 141–147.

    PubMed  Google Scholar 

  10. Pääbo, S., Poinar, H., Serre, D., et al., Genetic analyses from ancient DNA, Ann. Rev. Genet., 2004, vol. 38, pp. 645–679.

    PubMed  Google Scholar 

  11. Hofreiter, M., Serre, D., Poinar, H.N., et al., Ancient DNA, Nat. Rev. Genet., 2001, vol. 2, no. 5, pp. 353–359.

    CAS  PubMed  Google Scholar 

  12. Willerslev, E. and Cooper, A., Ancient DNA, Proc. Biol. Sci., 2005, vol. 272, no. 1558, pp. 3–16.

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Thomas, R.H., Schaffner, W., Wilson, A.C., and Pääbo, S., DNA phylogeny of the extinct marsupial wolf, Nature, 1989, vol. 340, no. 6233, pp. 465–467.

    CAS  PubMed  Google Scholar 

  14. Krajewski, C., Buckley, L., and Westerman, M., DNA phylogeny of the marsupial wolf resolved, Proc. Biol. Sci., 1997, vol. 264, no. 1383, pp. 911–917.

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Cooper, A., Lalueza-Fox, C., Anderson, S., et al., Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution, Nature, 2001, vol. 409, no. 6821, pp. 704–707.

    CAS  PubMed  Google Scholar 

  16. Greenwood, A.D., Castresana, J., Feldmaier-Fuchs, G., and Pääbo, S., A molecular phylogeny of two extinct sloths, Mol. Phylogenet. Evol., 2001, vol. 18, no. 1, pp. 94–103.

    CAS  PubMed  Google Scholar 

  17. Paxinos, E.E., James, H.F., Olson, S.L., et al., mtDNA from fossils reveals a radiation of Hawaiian geese recently derived from the Canada goose (Branta canadensis), Proc. Natl. Acad. Sci. U.S.A., 2002, vol. 99, no. 3, pp. 1399–1404.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Hanni, C., Laudet, V., Stehelin, D., and Taberlet, P., Tracking the origins of the cave bear (Ursus spelaeus) by mitochondrial DNA sequencing, Proc. Natl. Acad. Sci. U.S.A., 1994, vol. 91, no. 25, pp. 12336–12340.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Ramirez, O., Gigli, E., Bover, P., et al., Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean caprine, PLoS One, 2009, vol. 4, no. 5. e5670

    PubMed Central  PubMed  Google Scholar 

  20. Orlando, L., Calvignac, S., Schnebelen, C., et al., DNA from extinct giant lemurs links archaeolemurids to extant indriids, BMC Evol. Biol., 2008, vol. 8, p. 121.

    PubMed Central  PubMed  Google Scholar 

  21. Driscoll, C.A., Yamaguchi, N., Bar-Gal, G.K., et al., Mitochondrial phylogeography illuminates the origin of the extinct Caspian tiger and its relationship to the Amur tiger, PLoS One, 2009, vol. 4, no. 1. e4125

    PubMed Central  PubMed  Google Scholar 

  22. Thomas, W.K., Pääbo, S., Villablanca, F.X., and Wilson, A.C., Spatial and temporal continuity of kangaroo rat populations shown by sequencing mitochondrial DNA from museum specimens, J. Mol. Evol., 1990, vol. 31, no. 2, pp. 101–112.

    CAS  PubMed  Google Scholar 

  23. Pergams, O.R., Barnes, W.M., and Nyberg, D., Mammalian microevolution: rapid change in mouse mitochondrial DNA, Nature, 2003, vol. 423, no. 6938, p. 397.

    CAS  PubMed  Google Scholar 

  24. Hardy, C., Callou, C., Vigne, J.D., et al., Rabbit mitochondrial DNA diversity from prehistoric to modern times, J. Mol. Evol., 1995, vol. 40, no. 3, pp. 227–237.

    CAS  PubMed  Google Scholar 

  25. Hadly, E.A., Kohn, M.H., Leonard, J.A., and Wayne, R.K., A genetic record of population isolation in pocket gophers during Holocene climatic change, Proc. Natl. Acad. Sci. U.S.A., 1998, vol. 95, no. 12, pp. 6893–6896.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Wisely, S.M., Buskirk, S.W., Fleming, M.A., et al., Genetic diversity and fitness in black-footed ferrets before and during a bottleneck, J. Hered., 2002, vol. 93, no. 4, pp. 231–237.

    CAS  PubMed  Google Scholar 

  27. Larson, S., Jameson, R., Etnier, M., et al., Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries, Mol. Ecol., 2002, vol. 11, no. 10, pp. 1899–1903.

    CAS  PubMed  Google Scholar 

  28. Miller, C.R. and Waits, L.P., The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): implications for conservation, Proc. Natl. Acad. Sci. U.S.A., 2003, vol. 100, no. 7, pp. 4334–4339.

    CAS  PubMed Central  PubMed  Google Scholar 

  29. Hale, M.L., Lurz, P.W., Shirley, M.D., et al., Impact of landscape management on the genetic structure of red squirrel populations, Science, 2001, vol. 293, no. 5538, pp. 2246–2248.

    CAS  PubMed  Google Scholar 

  30. Verginelli, F., Capelli, C., Coia, V., et al., Mitochondrial DNA from prehistoric canids highlights relationships between dogs and South-East European wolves, Mol. Biol. Evol., 2005, vol. 22, no. 12, pp. 2541–2551.

    CAS  PubMed  Google Scholar 

  31. Lambert, D.M., Ritchie, P.A., Millar, C.D., et al., Rates of evolution in ancient DNA from Adelie penguins, Science, 2002, vol. 295, no. 5563, pp. 2270–2273.

    CAS  PubMed  Google Scholar 

  32. Dalen, L., Nystrom, V., Valdiosera, C., et al., Ancient DNA reveals lack of postglacial habitat tracking in the arctic fox, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, no. 16, pp. 6726–6729.

    CAS  PubMed Central  PubMed  Google Scholar 

  33. Debruyne, R., Chu, G., King, C.E., et al., Out of America: ancient DNA evidence for a new world origin of late quaternary woolly mammoths, Curr. Biol., 2008, vol. 18, no. 17, pp. 1320–1326.

    CAS  PubMed  Google Scholar 

  34. Krause, J., Unger, T., Nocon, A., et al., Mitochondrial genomes reveal an explosive radiation of extinct and extant bears near the Miocene-Pliocene boundary, BMC Evol. Biol., 2008, vol. 12, no. 8, pp. 220–232.

    Google Scholar 

  35. Leonard, J.A., Rohland, N., Glaberman, S., et al., A rapid loss of stripes: the evolutionary history of the extinct quagga, Biol. Lett., 2005, vol. 1, no. 3, pp. 291–295.

    PubMed Central  PubMed  Google Scholar 

  36. Steeves, T.E., Holdaway, R.N., Hale, M.L., et al., Merging ancient and modern DNA: extinct seabird taxon rediscovered in the North Tasman Sea, Biol. Lett., 2010, vol. 6, no. 1, pp. 94–97.

    PubMed Central  PubMed  Google Scholar 

  37. Seabrook-Davison, M., Huynen, L., Lambert, D.M., and Brunton, D.H., Ancient DNA resolves identity and phylogeny of New Zealand’s extinct and living quail (Coturnix sp.), PLoS One, 2009, vol. 4, no. 7.

    Google Scholar 

  38. Vorobieva, N.V., Sherbakov, D.Y., Druzhkova, A.S., et al., Genotyping of Capreolus pygargus fossil DNA from Denisova Cave reveals phylogenetic relationships between ancient and modern populations, PLoS One, 2011, vol. 6, no. 8.

    Google Scholar 

  39. Poinar, H.N., Hoss, M., Bada, J.L., and Pääbo, S., Amino acid racemization and the preservation of ancient DNA, Science, 1996, vol. 272, no. 5263, pp. 864–866.

    CAS  PubMed  Google Scholar 

  40. Smith, C.I., Chamberlain, A.T., Riley, M.S., et al., Neanderthal DNA: not just old but old and cold?, Nature, 2001, vol. 410, no. 6830, pp. 771–772.

    CAS  PubMed  Google Scholar 

  41. Lambert, J.B., Frue, J.S., and Pionar, G.O., Analysis of North American amber by carbon-13 NMR spectroscopy, Geoarcheology, 1990, vol. 5, pp. 43–52.

    CAS  Google Scholar 

  42. Hoss, M., Pääbo, S., and Vereshchagin, N.K., Mammoth DNA sequences, Nature, 1994, vol. 370, no. 6488, p. 333.

    CAS  PubMed  Google Scholar 

  43. Gilbert, M.T., Wilson, A.S., Bunce, M., et al., Ancient mitochondrial DNA from hair, Curr. Biol., 2004, vol. 14, no. 12, pp. R463–R464.

    CAS  PubMed  Google Scholar 

  44. Willerslev, E., Cappellini, E., Boomsma, W., et al., Ancient biomolecules from deep ice cores reveal a forested southern Greenland, Science, 2007, vol. 317, no. 5834, pp. 111–114.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Orlando, L., Ginolhac, A., Zhang, G., et al., Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse, Nature, 2013, vol. 499, no. 7456, pp. 74–78.

    CAS  PubMed  Google Scholar 

  46. Valdiosera, C., Garcia, N., Dalen, L., et al., Typing single polymorphic nucleotides in mitochondrial DNA as a way to access Middle Pleistocene DNA, Biol. Lett., 2006, vol. 2, no. 4, pp. 601–603.

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Dabney, J., Knapp, M., Glocke, I., et al., Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments, Proc. Natl. Acad. Sci. U.S.A., 2013, vol. 110, no. 39, pp. 15758–15763.

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Poinar, H., Kuch, M., McDonald, G., et al., Nuclear gene sequences from a Late Pleistocene sloth coprolite, Curr. Biol., 2003, vol. 13, no. 13, pp. 1150–1152.

    CAS  PubMed  Google Scholar 

  49. Willerslev, E. and Cooper, A., Ancient DNA, Proc. R. Soc. London, Ser. B, 2005, vol. 272, no. 1558, pp. 3–16.

    CAS  Google Scholar 

  50. Pääbo, S., Poinar, H., Serre, D., et al., Genetic analyses from ancient DNA, Annu. Rev. Genet., 2004, vol. 38, pp. 645–679.

    PubMed  Google Scholar 

  51. Hofreiter, M., Jaenicke, V., Serre, D., et al., DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA, Nucleic Acids Res., 2001, vol. 29, no. 23, pp. 4793–4799.

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Pusch, C.M., Giddings, I., and Scholz, M., Repair of degraded duplex DNA from prehistoric samples using Escherichia coli DNA polymerase I and T4 DNA ligase, Nucleic Acids Res., 1998, vol. 26, no. 3, pp. 857–859.

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Krause, J., Dear, P.H., Pollack, J.L., et al., Multiplex amplification of the mammoth mitochondrial genome and the evolution of Elephantidae, Nature, 2006, vol. 439, no. 7077, pp. 724–727.

    CAS  PubMed  Google Scholar 

  54. Vestheim, H. and Jarman, S.N., Blocking primers to enhance PCR amplification of rare sequences in mixed samples-a case study on prey DNA in Antarctic krill stomachs, Front Zool., 2008, vol. 5, pp. 12–19.

    PubMed Central  PubMed  Google Scholar 

  55. Gigli, E.R.M., Civit, S., Rosas, A., et al., An improved PCR method for endogenous DNA retrieval in contaminated Neanderthal samples based on the use of blocking primers, J. Archaeol. Sci., 2009, vol. 36, pp. 1466–1473.

    Google Scholar 

  56. Gilbert, M.T.P., Tomsho, L.P., Rendulic, S., et al., Whole-genome shotgun sequencing of mitochondria from ancient hair shafts, Science, 2007, vol. 317, no. 5846, pp. 1927–1930.

    CAS  PubMed  Google Scholar 

  57. Margulies, M., Egholm, M., Altman, W.E., et al., Genome sequencing in microfabricated high-density picolitre reactors, Nature, 2005, vol. 437, no. 7057, pp. 376–380.

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Metzker, M.L., Next generation technologies: basics and applications, Environ. Mol. Mutagen., 2010, vol. 51, no. 7, p. 691.

    Google Scholar 

  59. Ku, C.S. and Roukos, D.H., From next-generation sequencing to nanopore sequencing technology: paving the way to personalized genomic medicine, Expert Rev. Med. Devices, 2013, vol. 10, no. 1, pp. 1–6.

    CAS  PubMed  Google Scholar 

  60. Mardis, E.R., Next-generation DNA sequencing methods, Annu. Rev. Genomics Hum. Genet., 2008, vol. 9, pp. 387–402.

    CAS  PubMed  Google Scholar 

  61. Rothberg, J.M., Hinz, W., Rearick, T.M., et al., An integrated semiconductor device enabling non-optical genome sequencing, Nature, 2011, vol. 475, no. 7356, pp. 348–352.

    CAS  PubMed  Google Scholar 

  62. Natal’in, P.B. and Belyakin, S.N., Modern technologies of DNA sequencing in epigenetics, in Epigenetika (Epigenetics), Zakiyan, S.M., Vlasov, V.V., and Dement’eva, E.V., Eds., Novosibirsk: Sib. Otdel. Ross. Akad. Nauk, 2012, pp. 535–561.

    Google Scholar 

  63. Green, R.E., Krause, J., Briggs, A.W., et al., A draft sequence of the Neanderthal genome, Science, 2010, vol. 328, no. 5979, pp. 710–722.

    CAS  PubMed  Google Scholar 

  64. Reich, D., Green, R.E., Kircher, M., et al., Genetic history of an archaic hominin group from Denisova Cave in Siberia, Nature, 2010, vol. 468, no. 7327, pp. 1053–1060.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Gilbert, M.T.P., Rudbeck, L., Willerslev, E., et al., Biochemical and physical correlates of DNA contamination in archaeological human bones and teeth excavated at Matera, Italy, J. Archaeol. Sci., 2005, vol. 32, no. 5, pp. 785–793.

    Google Scholar 

  66. Rizzi, E., Lari, M., Gigli, E., et al., Ancient DNA studies: new perspectives on old samples, Genet. Sel. Evol., 2012, vol. 44, p. 21.

    CAS  PubMed Central  PubMed  Google Scholar 

  67. Gansauge, M.T. and Meyer, M., Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA, Nat. Protoc., 2013, vol. 8, no. 4, pp. 737–748.

    PubMed  Google Scholar 

  68. Gilbert, M.T., Binladen, J., Miller, W., et al., Recharacterization of ancient DNA miscoding lesions: insights in the era of sequencing-by-synthesis, Nucleic Acids Res., 2007, vol. 35, no. 1, pp. 1–10.

    CAS  PubMed Central  PubMed  Google Scholar 

  69. Stiller, M., Green, R.E., Ronan, M., et al., Patterns of nucleotide misincorporations during enzymatic amplification and direct large-scale sequencing of ancient DNA, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 37, pp. 13578–13584.

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Briggs, A.W., Stenzel, U., Johnson, P.L., et al., Patterns of damage in genomic DNA sequences from a Neanderthal, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, no. 37, pp. 14616–14621.

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Brotherton, P., Endicott, P., Sanchez, J.J., et al., 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., 2007, vol. 35, no. 17, pp. 5717–5728.

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Orlando, L., Ginolhac, A., Raghavan, M., et al., True single-molecule DNA sequencing of a Pleistocene horse bone, Genome Res., 2011, vol. 21, no. 10, pp. 1705–1719.

    CAS  PubMed Central  PubMed  Google Scholar 

  73. Summerer, D., Enabling technologies of genomicscale sequence enrichment for targeted high-throughput sequencing, Genomics, 2009, vol. 94, no. 6, pp. 363–368.

    CAS  PubMed  Google Scholar 

  74. Mamanova, L., Coffey, A.J., Scott, C.E., et al., Targetenrichment strategies for next-generation sequencing, Nat. Methods, 2010, vol. 7, no. 2, pp. 111–118.

    CAS  PubMed  Google Scholar 

  75. Stiller, M., Knapp, M., Stenzel, U., et al., Direct multiplex sequencing (DMPS)-a novel method for targeted high-throughput sequencing of ancient and highly degraded DNA, Genome Res., 2009, vol. 19, no. 10, pp. 1843–1848.

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Briggs, A.W., Good, J.M., Green, R.E., et al., Targeted retrieval and analysis of five Neanderthal mtDNA genomes, Science, 2009, vol. 325, no. 5938, pp. 318–321.

    CAS  PubMed  Google Scholar 

  77. Maricic, T., Whitten, M., and Pääbo, S., Multiplexed DNA sequence capture of mitochondrial genomes using PCR products, PLoS One, 2010, vol. 5, no. 11. e14004

    PubMed Central  PubMed  Google Scholar 

  78. Gnirke, A., Melnikov, A., Maguire, J., et al., Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing, Nat. Biotechnol., 2009, vol. 27, no. 2, pp. 182–189.

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Avila-Arcos, M.C., Cappellini, E., Romero-Navarro, J.A., et al., Application and comparison of large-scale solution-based DNA capture-enrichment methods on ancient DNA, Sci. Rep., 2011, vol. 1, p. 74.

    PubMed Central  PubMed  Google Scholar 

  80. Bos, K.I., Schuenemann, V.J., Golding, G.B., et al., A draft genome of Yersinia pestis from victims of the black death, Nature, 2011, vol. 478, no. 7370, pp. 506–510.

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Burbano, H.A., Hodges, E., Green, R.E., et al., Targeted investigation of the Neanderthal genome by array-based sequence capture, Science, 2010, vol. 328, no. 5979, pp. 723–725.

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Paijmans, J.L., Gilbert, M.T., and Hofreiter, M., Mitogenomic analyses from ancient DNA, Mol. Phylogenet. Evol., 2013, vol. 69, no. 2, pp. 404–416.

    CAS  PubMed  Google Scholar 

  83. Ginolhac, A., Vilstrup, J., Stenderup, J., et al., Improving the performance of true single molecule sequencing for ancient DNA, BMC Genomics, 2012, vol. 13, p. 177.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Hagelberg, E., Thomas, M.G., Cook, C.E., Jr., et al., DNA from ancient mammoth bones, Nature, 1994, vol. 370, no. 6488, pp. 333–334.

    CAS  PubMed  Google Scholar 

  85. Barriel, V., Thuet, E., and Tassy, P., Molecular phylogeny of Elephantidae: extreme divergence of the extant forest African elephant, C. R. Acad. Sci. III, 1999, vol. 322, no. 6, pp. 447–454.

    CAS  PubMed  Google Scholar 

  86. Debruyne, R., Barriel, V., and Tassy, P., Mitochondrial cytochrome b of the Lyakhov mammoth (Proboscidea, Mammalia): new data and phylogenetic analyses of Elephantidae, Mol. Phylogenet. Evol., 2003, vol. 26, no. 3, pp. 421–434.

    CAS  PubMed  Google Scholar 

  87. Thomas, M.G., Hagelberg, E., Jone, H.B., et al., Molecular and morphological evidence on the phylogeny of the Elephantidae, Proc. Biol. Sci., 2000, vol. 267, no. 1461, pp. 2493–2500.

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Ozawa, T., Hayashi, S., and Mikhelson, V.M., Phylogenetic position of Mammoth and Steller’s sea cow within Tethytheria demonstrated by mitochondrial DNA sequences, J. Mol. Evol., 1997, vol. 44, no. 4, pp. 406–413.

    CAS  PubMed  Google Scholar 

  89. Rohland, N., Reich, D., Mallick, S., et al., Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants, PLoS Biol., 2010, vol. 8, no. 12. e1000564

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Phillips, M.J., Gibb, G.C., Crimp, E.A., and Penny, D., Tinamous and moa flock together: mitochondrial genome sequence analysis reveals independent losses of flight among ratites, Syst. Biol., 2010, vol. 59, no. 1, pp. 90–107.

    PubMed  Google Scholar 

  91. Bon, C., Berthonaud, V., Maksud, F., et al., Coprolites as a source of information on the genome and diet of the cave hyena, Proc. Biol. Sci., 2012, vol. 279, no. 1739, pp. 2825–2830.

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Miller, W., Drautz, D.I., Janecka, J.E., et al., The mitochondrial genome sequence of the Tasmanian tiger (Thylacinus cynocephalus), Genome Res., 2009, vol. 19, no. 2, pp. 213–220.

    CAS  PubMed Central  PubMed  Google Scholar 

  93. Orlando, L., Leonard, J.A., Thenot, A., et al., Ancient DNA analysis reveals woolly rhino evolutionary relationships, Mol. Phylogenet. Evol., 2003, vol. 28, no. 3, pp. 485–499.

    CAS  PubMed  Google Scholar 

  94. Willerslev, E., Gilbert, M.T., Binladen, J., et al., Analysis of complete mitochondrial genomes from extinct and extant rhinoceroses reveals lack of phylogenetic resolution, BMC Evol. Biol., 2009, vol. 9, p. 95.

    PubMed Central  PubMed  Google Scholar 

  95. Lindqvist, C., Schuster, S.C., Sun, Y., et al., Complete mitochondrial genome of a Pleistocene jawbone unveils the origin of polar bear, Proc. Natl. Acad. Sci. U.S.A., 2010, vol. 107, no. 11, pp. 5053–5057.

    CAS  PubMed Central  PubMed  Google Scholar 

  96. Shields, G.F., Adams, D., Garner, G., et al., Phylogeography of mitochondrial DNA variation in brown bears and polar bears, Mol. Phylogenet. Evol., 2000, vol. 15, no. 2, pp. 319–326.

    CAS  PubMed  Google Scholar 

  97. Hailer, F., Kutschera, V.E., Hallstrom, B.M., et al., Nuclear genomic sequences reveal that polar bears are an old and distinct bear lineage, Science, 2012, vol. 336, no. 6079, pp. 344–347.

    CAS  PubMed  Google Scholar 

  98. Edwards, C.J., Suchard, M.A., Lemey, P., et al., Ancient hybridization and an Irish origin for the modern polar bear matriline, Curr. Biol., 2011, vol. 21, no. 15, pp. 1251–1258.

    CAS  PubMed  Google Scholar 

  99. Enk, J., Devault, A., Debruyne, R., et al., Complete Columbian mammoth mitogenome suggests interbreeding with woolly mammoths, Genome Biol., 2011, vol. 12, no. 5, p. R51.

    PubMed Central  PubMed  Google Scholar 

  100. Debruyne, R., A case study of apparent conflict between molecular phylogenies: the interrelationships of African elephants, Cladistics, 2005, vol. 21, no. 1, pp. 31–50.

    Google Scholar 

  101. Ho, S.Y., Kolokotronis, S.O., and Allaby, R.G., Elevated substitution rates estimated from ancient DNA sequences, Biol. Lett., 2007, vol. 3, no. 6, pp. 702–705.

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Ho, S.Y., Shapiro, B., Phillips, M.J., et al., Evidence for time dependency of molecular rate estimates, Syst. Biol., 2007, vol. 56, no. 3, pp. 515–522.

    PubMed  Google Scholar 

  103. Brown, W.M., George, M., Jr., and Wilson, A.C., Rapid evolution of animal mitochondrial DNA, Proc. Natl. Acad. Sci. U.S.A., 1979, vol. 76, no. 4, pp. 1967–1971.

    CAS  PubMed Central  PubMed  Google Scholar 

  104. Subramanian, S., Denver, D.R., Millar, C.D., et al., High mitogenomic evolutionary rates and time dependency, Trends Genet., 2009, vol. 25, no. 11, pp. 482–486.

    CAS  PubMed  Google Scholar 

  105. Lerner, H.R., Meyer, M., James, H.F., et al., Multilocus resolution of phylogeny and timescale in the extant adaptive radiation of Hawaiian honeycreepers, Curr. Biol., 2011, vol. 21, no. 21, pp. 1838–1844.

    CAS  PubMed  Google Scholar 

  106. Bailey, J.F., Richards, M.B., Macaulay, V.A., et al., Ancient DNA suggests a recent expansion of European cattle from a diverse wild progenitor species, Proc. Biol. Sci., 1996, vol. 263, no. 1376, pp. 1467–1473.

    CAS  PubMed  Google Scholar 

  107. Troy, C.S., Machugh, D.E., Bailey, J.F., et al., Genetic evidence for Near-Eastern origins of European cattle, Nature, 2001, vol. 410, no. 6832, pp. 1088–1091.

    CAS  PubMed  Google Scholar 

  108. Anderung, C., Bouwman, A., Persson, P., et al., Prehistoric contacts over the Straits of Gibraltar indicated by genetic analysis of Iberian bronze age cattle, Proc. Natl. Acad. Sci. U.S.A., 2005, vol. 102, no. 24, pp. 8431–8435.

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Beja-Pereira, A., Caramelli, D., Lalueza-Fox, C., et al., The origin of European cattle: evidence from modern and ancient DNA, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 21, pp. 8113–8118.

    CAS  PubMed Central  PubMed  Google Scholar 

  110. Bollongino, R., Edwards, C.J., Alt, K.W., et al., Early history of European domestic cattle as revealed by ancient DNA, Biol. Lett., 2006, vol. 2, no. 1, pp. 155–159.

    CAS  PubMed Central  PubMed  Google Scholar 

  111. Edwards, C.J., Bollongino, R., Scheu, A., et al., Mitochondrial DNA analysis shows a Near Eastern Neolithic origin for domestic cattle and no indication of domestication of European aurochs, Proc. Biol. Sci., 2007, vol. 274, no. 1616, pp. 1377–1385.

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Mona, S., Catalano, G., Lari, M., et al., Population dynamic of the extinct European aurochs: genetic evidence of a north-south differentiation pattern and no evidence of post-glacial expansion, BMC Evol. Biol., 2010, vol. 10, p. 83.

    PubMed Central  PubMed  Google Scholar 

  113. Achilli, A., Olivieri, A., Pellecchia, M., et al., Mitochondrial genomes of extinct aurochs survive in domestic cattle, Curr. Biol., 2008, vol. 18, no. 4, pp. R157–R158.

    CAS  PubMed  Google Scholar 

  114. Achilli, A., Bonfiglio, S., Olivieri, A., et al., The multifaceted origin of taurine cattle reflected by the mitochondrial genome, PLoS One, 2009, vol. 4, no. 6. e5753

    PubMed Central  PubMed  Google Scholar 

  115. Bonfiglio, S., Achilli, A., Olivieri, A., et al., The enigmatic origin of bovine mtDNA haplogroup R: sporadic interbreeding or an independent event of Bos primigenius domestication in Italy?, PLoS One, 2010, vol. 5, no. 12. e15760

    CAS  PubMed Central  PubMed  Google Scholar 

  116. Greenwood, A.D., Capelli, C., Possnert, G., and Pääbo, S., Nuclear DNA sequences from Late Pleistocene megafauna, Mol. Biol. Evol., 1999, vol. 16, no. 11, pp. 1466–1473.

    CAS  PubMed  Google Scholar 

  117. Jaenicke-Despres, V., Buckler, E.S., Smith, B.D., et al., Early allelic selection in maize as revealed by ancient DNA, Science, 2003, vol. 302, no. 5648, pp. 1206–1208.

    CAS  PubMed  Google Scholar 

  118. Bunce, M., Worthy, T.H., Ford, T., et al., Extreme reversed sexual size dimorphism in the extinct New Zealand moa Dinornis, Nature, 2003, vol. 425, no. 6954, pp. 172–175.

    CAS  PubMed  Google Scholar 

  119. Huynen, L., Millar, C.D., Scofield, R.P., and Lambert, D.M., Nuclear DNA sequences detect species limits in ancient moa, Nature, 2003, vol. 425, no. 6954, pp. 175–178.

    CAS  PubMed  Google Scholar 

  120. Bollongino, R., Elsner, J., Vigne, J.D., and Burger, J., Y-SNPs do not indicate hybridization between European aurochs and domestic cattle, PLoS One, 2008, vol. 3, no. 10. e3418

    PubMed Central  PubMed  Google Scholar 

  121. Gotherstrom, A., Anderung, C., Hellborg, L., et al., Cattle domestication in the Near East was followed by hybridization with aurochs bulls in Europe, Proc. Biol. Sci., 2005, vol. 272, no. 1579, pp. 2345–2350.

    PubMed Central  PubMed  Google Scholar 

  122. Larson, G., Dobney, K., Albarella, U., et al., Worldwide phylogeography of wild boar reveals multiple centers of pig domestication, Science, 2005, vol. 307, no. 5715, pp. 1618–1621.

    CAS  PubMed  Google Scholar 

  123. Larson, G., Albarella, U., Dobney, K., et al., Ancient DNA, pig domestication, and the spread of the Neolithic into Europe, Proc. Natl. Acad. Sci. U.S.A., 2007, vol. 104, no. 39, pp. 15276–15281.

    PubMed Central  PubMed  Google Scholar 

  124. Vila, C., Leonard, J.A., Gotherstrom, A., et al., Widespread origins of domestic horse lineages, Science, 2001, vol. 291, no. 5503, pp. 474–477.

    CAS  PubMed  Google Scholar 

  125. Cieslak, M., Pruvost, M., Benecke, N., et al., Origin and history of mitochondrial DNA lineages in domestic horses, PLoS One, 2010, vol. 5, no. 12. e15311

    CAS  PubMed Central  PubMed  Google Scholar 

  126. Pang, J.F., Kluetsch, C., Zou, X.J., et al., mtDNA data indicate a single origin for dogs south of Yangtze River, less than 16300 years ago, from numerous wolves, Mol. Biol. Evol., 2009, vol. 26, no. 12, pp. 2849–2864.

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Druzhkova, A.S., Thalmann, O., Trifonov, V.A., et al., Ancient DNA analysis affirms the canid from Altai as a primitive dog, PLoS One, 2013, vol. 8, no. 3. e57754

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Thalmann, O., Shapiro, B., Cui, P., et al., Complete mitochondrial genomes of ancient canids suggest a European origin of domestic dogs, Science, 2013, vol. 342, no. 6160, pp. 871–874.

    CAS  PubMed  Google Scholar 

  129. Brown, T.A., Allaby, R.G., Brown, K.A., and Jones, M.K., Biomolecular archaeology of wheat: past, present and future, World Archaeol., 1993, vol. 25, no. 1, pp. 64–73.

    CAS  PubMed  Google Scholar 

  130. Brown, T.A., Allaby, R.G., Brown, K.A., et al., DNA in wheat seeds from European archaeological sites, Experientia, 1994, vol. 50, no. 6, pp. 571–575.

    CAS  PubMed  Google Scholar 

  131. Jones, M. and Brown, T., Agricultural origins: the evidence of modern and ancient DNA, Holocene, 2000, vol. 10, no. 6, pp. 769–776.

    Google Scholar 

  132. Parducci, L. and Petit, R.J., Ancient DNA-unlocking plants’ fossil secrets, New Phytol., 2004, vol. 161, no. 2, pp. 335–339.

    Google Scholar 

  133. Bennett, K.D. and Parducci, L., DNA from pollen: principles and potential, Holocene, 2006, vol. 16, no. 8, pp. 1031–1034.

    Google Scholar 

  134. Wang, R.L., Stec, A., Hey, J., et al., The limits of selection during maize domestication, Nature, 1999, vol. 398, no. 6724, pp. 236–239.

    CAS  PubMed  Google Scholar 

  135. Whitt, S.R., Wilson, L.M., Tenaillon, M.I., et al., Genetic diversity and selection in the maize starch pathway, Proc. Natl. Acad. Sci. U.S.A., 2002, vol. 99, no. 20, pp. 12959–12962.

    CAS  PubMed Central  PubMed  Google Scholar 

  136. Wang, H., Nussbaum-Wagler, T., Li, B.L., et al., The origin of the naked grains of maize, Nature, 2005, vol. 436, no. 7051, pp. 714–719.

    CAS  PubMed Central  PubMed  Google Scholar 

  137. Vouillamoz, J.F. and Grando, M.S., Genealogy of wine grape cultivars: “Pinot” is related to “Syrah,” Heredity, 2006, vol. 97, no. 2, pp. 102–110.

    CAS  PubMed  Google Scholar 

  138. Witas, H.W., Tomczyk, J., Jedrychowska-Danska, K., et al., mtDNA from the early Bronze Age to the Roman period suggests a genetic link between the Indian subcontinent and Mesopotamian cradle of civilization, PLoS One, 2013, vol. 8, no. 9. e73682

    CAS  PubMed Central  PubMed  Google Scholar 

  139. Rasmussen, M., Guo, X., Wang, Y., et al., An aboriginal Australian genome reveals separate human dispersals into Asia, Science, 2011, vol. 334, no. 6052, pp. 94–98.

    CAS  PubMed Central  PubMed  Google Scholar 

  140. Vernesi, C., Caramelli, D., Dupanloup, I., et al., The Etruscans: a population-genetic study, Am. J. Hum. Genet., 2004, vol. 74, no. 4, pp. 694–704.

    CAS  PubMed Central  PubMed  Google Scholar 

  141. Guimaraes, S., Ghirotto, S., Benazzo, A., et al., Genealogical discontinuities among Etruscan, Medieval, and contemporary Tuscans, Mol. Biol. Evol., 2009, vol. 26, no. 9, pp. 2157–2166.

    CAS  PubMed  Google Scholar 

  142. Endicott, P., Gilbert, M.T., Stringer, C., et al., The genetic origins of the Andaman islanders, Am. J. Hum. Genet., 2003, vol. 72, no. 1, pp. 178–184.

    CAS  PubMed Central  PubMed  Google Scholar 

  143. Caramelli, D., Lalueza-Fox, C., Capelli, C., et al., Genetic analysis of the skeletal remains attributed to Francesco Petrarca, Forensic Sci. Int., 2007, vol. 173, no. 1, pp. 36–40.

    CAS  PubMed  Google Scholar 

  144. Sampietro, M.L., Caramelli, D., Lao, O., et al., The genetics of the pre-Roman Iberian Peninsula: a mtDNA study of ancient Iberians, Ann. Hum. Genet., 2005, vol. 69, vol. 5, pp. 535–548.

    CAS  PubMed  Google Scholar 

  145. Haak, W., Forster, P., Bramanti, B., et al., Ancient DNA from the first European farmers in 7500-year-old Neolithic sites, Science, 2005, vol. 310, no. 5750, pp. 1016–1018.

    CAS  PubMed  Google Scholar 

  146. Bramanti, B., Thomas, M.G., Haak, W., et al., Genetic discontinuity between local hunter-gatherers and central Europe’s first farmers, Science, 2009, vol. 326, no. 5949, pp. 137–140.

    CAS  PubMed  Google Scholar 

  147. Haak, W.B.O., Sanchez, J.J., Koshel, S., et al., Members of the Genographic Consortium: ancient DNA from European early Neolithic farmers reveals their near eastern affinities, PLoS Biol., 2010, vol. 8. e1000536

    PubMed Central  PubMed  Google Scholar 

  148. Malmstrom, H., Gilbert, M.T., Thomas, M.G., et al., Ancient DNA reveals lack of continuity between Neolithic hunter-gatherers and contemporary Scandinavians, Curr. Biol., 2009, vol. 19, no. 20, pp. 1758–1762.

    PubMed  Google Scholar 

  149. Krause, J., Briggs, A.W., Kircher, M., et al., A complete mtDNA genome of an early modern human from Kostenki, Russia, Curr. Biol., 2010, vol. 20, no. 3, pp. 231–236.

    CAS  Google Scholar 

  150. Ermini, L., Olivieri, C., Rizzi, E., et al., Complete mitochondrial genome sequence of the Tyrolean Iceman, Curr. Biol., 2008, vol. 18, no. 21, pp. 1687–1693.

    CAS  PubMed  Google Scholar 

  151. Gibbons, A., Human evolution: oldest Homo sapiens genome pinpoints Neanderthal input, Science, 2014, vol. 343, no. 6178, p. 1417.

    PubMed  Google Scholar 

  152. Gilbert, M.T., Kivisild, T., Gronnow, B., et al., Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland, Science, 2008, vol. 320, no. 5884, pp. 1787–1789.

    CAS  PubMed  Google Scholar 

  153. Rasmussen, M., Li, Y.R., Lindgreen, S., et al., Ancient human genome sequence of an extinct palaeo-Eskimo, Nature, 2010, vol. 463, no. 7282, pp. 757–762.

    CAS  PubMed Central  PubMed  Google Scholar 

  154. Cui, Y., Lindo, J., Hughes, C.E., et al., Ancient DNA analysis of mid-Holocene individuals from the Northwest Coast of North America reveals different evolutionary paths for mitogenomes, PLoS One, 2013, vol. 8, no. 7. e66948

    CAS  PubMed Central  PubMed  Google Scholar 

  155. Evans, P.D., Gilbert, S.L., Mekel-Bobrov, N., et al., Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans, Science, 2005, vol. 309, no. 5741, pp. 1717–1720.

    CAS  PubMed  Google Scholar 

  156. Evans, P.D., Mekel-Bobrov, N., Vallender, E.J., et al., Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, no. 48, pp. 18178–18183.

    CAS  PubMed Central  PubMed  Google Scholar 

  157. Green, R.E., Krause, J., Ptak, S.E., et al., Analysis of one million base pairs of Neanderthal DNA, Nature, 2006, vol. 444, no. 7117, pp. 330–336.

    CAS  PubMed  Google Scholar 

  158. Noonan, J.P., Coop, G., Kudaravalli, S., et al., Sequencing and analysis of Neanderthal genomic DNA, Science, 2006, vol. 314, no. 5802, pp. 1113–1118.

    CAS  PubMed Central  PubMed  Google Scholar 

  159. Wall, J.D. and Kim, S.K., Inconsistencies in Neanderthal genomic DNA sequences, PLoS Genet., 2007, vol. 3, no. 10, pp. 1862–1866.

    CAS  PubMed  Google Scholar 

  160. Krause, J., Lalueza-Fox, C., Orlando, L., et al., The derived FOXP2 variant of modern humans was shared with Neanderthals, Curr. Biol., 2007, vol. 17, no. 21, pp. 1908–1912.

    CAS  PubMed  Google Scholar 

  161. Krause, J., Fu, Q., Good, J.M., et al., The complete mitochondrial DNA genome of an unknown hominin from southern Siberia, Nature, 2010, vol. 464, no. 7290, pp. 894–897.

    CAS  PubMed  Google Scholar 

  162. Briggs, A.W., Rapid retrieval of DNA target sequences by primer extension capture, Methods Mol. Biol., 2011, vol. 772, pp. 145–154.

    CAS  PubMed  Google Scholar 

  163. Lalueza-Fox, C. and Gilbert, M.T., Paleogenomics of archaic hominins, Curr. Biol., 2011, vol. 21, no. 24, pp. R1002–R1009.

    CAS  PubMed  Google Scholar 

  164. Meyer, M., Kircher, M., Gansauge, M.T., et al., A high-coverage genome sequence from an archaic Denisovan individual, Science, 2012, vol. 338, no. 6104, pp. 222–226.

    CAS  PubMed Central  PubMed  Google Scholar 

  165. Gokcumen, O., Zhu, Q., Mulder, L.C., et al., Balancing selection on a regulatory region exhibiting ancient variation that predates human-Neanderthal divergence, PLoS Genet., 2013, vol. 9, no. 4. e1003404

    CAS  PubMed Central  PubMed  Google Scholar 

  166. Guojie, Z., Zhang, P., Michael, K., et al., Triangulation of the human, chimpanzee, and Neanderthal genome sequences identifies potentially compensated mutations, Hum. Mutat., 2010, vol. 31, no. 12, pp. 1286–1293.

    Google Scholar 

  167. Guojie, Z., Zhang, P., Edward, V.B., et al., Crosscomparison of the genome sequences from human, chimpanzee, Neanderthal and a Denisovan hominin identifies novel potentially compensated mutations, Hum. Genomics, 2011, vol. 5, no. 5, pp. 453–484.

    Google Scholar 

  168. Huerta-Sanchez, E., Jin, X., Asan, et al., Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA, Nature, 2014, vol. 512, no. 7513, pp. 194–197.

    CAS  PubMed Central  PubMed  Google Scholar 

  169. Anastasiou, E. and Mitchell, P.D., Palaeopathology and genes: investigating the genetics of infectious diseases in excavated human skeletal remains and mummies from past populations, Gene, 2013, vol. 528, no. 1, pp. 33–40.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. S. Graphodatsky.

Additional information

Original Russian Text © A.S. Druzhkova, N.V. Vorobieva, V.A. Trifonov, A.S. Graphodatsky, 2015, published in Genetika, 2015, Vol. 51, No. 6, pp. 627–643.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Druzhkova, A.S., Vorobieva, N.V., Trifonov, V.A. et al. Ancient DNA: Results and prospects (The 30th anniversary). Russ J Genet 51, 529–544 (2015). https://doi.org/10.1134/S1022795415060046

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1022795415060046

Keywords

  • Mitochondrial Genome
  • Polar Bear
  • Modern Human
  • Complete Mitochondrial Genome
  • African Elephant