Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Harnessing ancient genomes to study the history of human adaptation

Key Points

  • Ancient DNA provides transformative insight into the history of human adaptation via the ability to directly track genetic variant frequency changes across space and time.

  • Analyses of human, archaic hominin, and domesticated plant and animal ancient genomic data sets can each inform our understanding of past human evolution and behaviour.

  • The number of published ancient genomic data sets is growing substantially each year, contributing expanded precision and power to evolutionary analyses based on these data.

  • Human ancient genome data have already helped characterize the histories of biological adaptations to northern latitudes and cold climates, agriculture-associated dietary shifts, and a changing infectious disease landscape.

  • After migrating out of Africa, ancient human populations acquired genetic variants conferring fitness advantages in Eurasian environments through adaptive introgression with archaic hominin populations who had already been inhabiting this region for hundreds of thousands of years.

  • Ancient genome data reveal some substantial time lags between documented environmental or cultural changes and the appearance and spread of genetic variants associated with human biological adaptations, with possible implications for intervening human health and/or potential compensatory cultural behaviours.


The past several years have witnessed an explosion of successful ancient human genome-sequencing projects, with genomic-scale ancient DNA data sets now available for more than 1,100 ancient human and archaic hominin (for example, Neandertal) individuals. Recent 'evolution in action' analyses have started using these data sets to identify and track the spatiotemporal trajectories of genetic variants associated with human adaptations to novel and changing environments, agricultural lifestyles, and introduced or co-evolving pathogens. Together with evidence of adaptive introgression of genetic variants from archaic hominins to humans and emerging ancient genome data sets for domesticated animals and plants, these studies provide novel insights into human evolution and the evolutionary consequences of human behaviour that go well beyond those that can be obtained from modern genomic data or the fossil and archaeological records alone.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: The recent (and ongoing) ancient genomic explosion.
Figure 2: Ancient genomic signatures of positive natural selection.
Figure 3: Biocultural adaptation to dairying and milk consumption.
Figure 4: Adaptive archaic introgression.
Figure 5: Insights into the timing of different trait evolution processes for domesticated species based on ancient DNA.


  1. 1

    Huxley, T. H. Evidence as to Man's Place in Nature (Williams and Norgate, 1863).

    Google Scholar 

  2. 2

    Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).

    Book  Google Scholar 

  3. 3

    Fan, S., Hansen, M. E. B., Lo, Y. & Tishkoff, S. A. Going global by adapting local: A review of recent human adaptation. Science 354, 54–59 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. 4

    Laland, K. N., Odling-Smee, J. & Myles, S. How culture shaped the human genome: bringing genetics and the human sciences together. Nat. Rev. Genet. 11, 137–148 (2010).

    CAS  Article  Google Scholar 

  5. 5

    Scheinfeldt, L. B. & Tishkoff, S. A. Recent human adaptation: genomic approaches, interpretation and insights. Nat. Rev. Genet. 14, 692–702 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  6. 6

    Sabeti, P. C. et al. Positive natural selection in the human lineage. Science 312, 1614–1620 (2006).

    CAS  Article  Google Scholar 

  7. 7

    Raj, T. et al. Common risk alleles for inflammatory diseases are targets of recent positive selection. Am. J. Hum. Genet. 92, 517–529 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8

    Papandreou, I., Cairns, R. A., Fontana, L., Lim, A. L. & Denko, N. C. HIF-1 mediates adaptation to hypoxia by actively downregulating mitochondrial oxygen consumption. Cell Metab. 3, 187–197 (2006).

    CAS  Article  Google Scholar 

  9. 9

    Natarajan, V. T. et al. IFN-γ signaling maintains skin pigmentation homeostasis through regulation of melanosome maturation. Proc. Natl Acad. Sci. USA 111, 2301–2306 (2014).

    CAS  Article  Google Scholar 

  10. 10

    Norton, H. L. et al. Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol. Biol. Evol. 24, 710–722 (2006).

    Article  CAS  Google Scholar 

  11. 11

    Pickrell, J. K. & Reich, D. Toward a new history and geography of human genes informed by ancient DNA. Trends Genet. 30, 377–389 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  12. 12

    Nielsen, R. et al. Tracing the peopling of the world through genomics. Nature 541, 302–310 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13

    Orlando, L., Gilbert, M. T. P. & Willerslev, E. Reconstructing ancient genomes and epigenomes. Nat. Rev. Genet. 16, 395–408 (2015).

    CAS  Article  Google Scholar 

  14. 14

    Llamas, B., Willerslev, E. & Orlando, L. Human evolution: a tale from ancient genomes. Phil. Trans. R. Soc. B 372, 20150484 (2016).

    Article  CAS  Google Scholar 

  15. 15

    Nakagome, S. et al. Estimating the ages of selection signals from different epochs in human history. Mol. Biol. Evol. 33, 657–669 (2016).

    CAS  Article  Google Scholar 

  16. 16

    Field, Y. et al. Detection of human adaptation during the past 2000 years. Science 354, 760–764 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  17. 17

    Malaspinas, A.-S., Malaspinas, O., Evans, S. N. & Slatkin, M. Estimating allele age and selection coefficient from time-serial data. Genetics 192, 599–607 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18

    Sams, A. J., Hawks, J. & Keinan, A. The utility of ancient human DNA for improving allele age estimates, with implications for demographic models and tests of natural selection. J. Hum. Evol. 79, 64–72 (2015).

    Article  Google Scholar 

  19. 19

    Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20

    Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015). This paper performed a genome-wide scan for signatures of positive selection with ancient genome data from 230 Europeans (!8,500–2,300 years BP ) and characterized the spatiotemporal frequency trajectories of adaptive alleles related to diet, skin pigmentation, stature and the immune response.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. 21

    Gelabert, P., Olalde, I., de-Dios, T., Civit, S. & Lalueza-Fox, C. Malaria was a weak selective force in ancient Europeans. Sci. Rep. 7, 1377 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  22. 22

    Buckley, M. T. et al. Selection in Europeans on fatty acid desaturases associated with dietary changes. Mol. Biol. Evol. 34, 1307–1318 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23

    Ye, K., Gao, F., Wang, D., Bar-Yosef, O. & Keinan, A. Dietary adaptation of FADS genes in Europe varied across time and geography. Nat. Ecol. Evol. 1, 0167 (2017).

    Article  Google Scholar 

  24. 24

    Sverrisdóttir, O. Ó. et al. Direct estimates of natural selection in Iberia indicate calcium absorption was not the only driver of lactase persistence in Europe. Mol. Biol. Evol. 31, 975–983 (2014).

    Article  CAS  Google Scholar 

  25. 25

    Günther, T. et al. Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. Preprint at bioRxiv (2017). This study conducted a genome-wide scan of positive selection using ancient genome data from seven Scandinavian individuals (!9,500–6,000 years BP ) to reveal a haplotype that the authors propose may underlie physiological adaptation to cold climate.

  26. 26

    Stephan, W. Signatures of positive selection: from selective sweeps at individual loci to subtle allele frequency changes in polygenic adaptation. Mol. Ecol. 25, 79–88 (2016).

    CAS  Article  Google Scholar 

  27. 27

    Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).

    CAS  Article  Google Scholar 

  28. 28

    Haak, W. et al. Massive migration from the steppe was a source for Indo–European languages in Europe. Nature 522, 207–211 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29

    Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Preprint at bioRxiv (2017).

  30. 30

    Cassidy, L. M. et al. Neolithic and Bronze Age migration to Ireland and establishment of the insular Atlantic genome. Proc. Natl Acad. Sci. USA 113, 368–373 (2016).

    CAS  Article  Google Scholar 

  31. 31

    Shennan, S. Evolutionary demography and the population history of the European early Neolithic. Hum. Biol. 81, 339–355 (2009).

    Article  Google Scholar 

  32. 32

    Leonardi, M. et al. Evolutionary patterns and processes: lessons from ancient DNA. Syst. Biol. 66, e1–e29 (2017).

    Google Scholar 

  33. 33

    Mirazón Lahr, M. The shaping of human diversity: filters, boundaries and transitions. Phil. Trans. R. Soc. B 371, (2016).

  34. 34

    Stewart, J. R. & Stringer, C. B. Human evolution out of Africa: the role of refugia and climate change. Science 335, 1317–1321 (2012).

    CAS  Article  Google Scholar 

  35. 35

    Richards, M. A brief review of the archaeological evidence for Palaeolithic and Neolithic subsistence. Eur. J. Clin. Nutr. 56, 1262–1278 (2002).

    Article  Google Scholar 

  36. 36

    Perry, G. H. Parasites and human evolution. Evol. Anthropol. 23, 218–228 (2014).

    Article  Google Scholar 

  37. 37

    Pearce-Duvet, J. M. C. The origin of human pathogens: evaluating the role of agriculture and domestic animals in the evolution of human disease. Biol. Rev. 81, 369–382 (2006).

    Article  Google Scholar 

  38. 38

    Jablonski, N. G. & Chaplin, G. Human skin pigmentation as an adaptation to UV radiation. Proc. Natl Acad. Sci. USA 107, 8962–8968 (2010).

    CAS  Article  Google Scholar 

  39. 39

    Chaplin, G. & Jablonski, N. G. Vitamin D and the evolution of human depigmentation. Am. J. Phys. Anthropol. 139, 451–461 (2009).

    Article  Google Scholar 

  40. 40

    Brickley, M. B. et al. Ancient vitamin D deficiency: long-term trends. Curr. Anthropol. 58, 420–427 (2017).

    Article  Google Scholar 

  41. 41

    Ovesen, L., Brot, C. & Jakobsen, J. Food contents and biological activity of 25-hydroxyvitamin D: a vitamin D metabolite to be reckoned with? Ann. Nutr. Metab. 47, 107–113 (2003).

    CAS  Article  Google Scholar 

  42. 42

    Bodnar, L. M. et al. Maternal vitamin D deficiency increases the risk of preeclampsia. J. Clin. Endocrinol. Metab. 92, 3517–3522 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43

    Wang, T. J. et al. Common genetic determinants of vitamin D insufficiency: a genome-wide association study. Lancet 376, 180–188 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44

    Lao, O., de Gruijter, J. M., van Duijn, K., Navarro, A. & Kayser, M. Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann. Hum. Genet. 71, 354–369 (2007).

    CAS  Article  Google Scholar 

  45. 45

    Sturm, R. A. et al. Human pigmentation genes under environmental selection. Genome Biol. 13, 248–263 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46

    Beleza, S. et al. The timing of pigmentation lightening in Europeans. Mol. Biol. Evol. 30, 24–35 (2013).

    CAS  Article  Google Scholar 

  47. 47

    Günther, T. et al. Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques. Proc. Natl Acad. Sci. USA 112, 11917–11922 (2015).

    Article  CAS  Google Scholar 

  48. 48

    González-Fortes, G. et al. Paleogenomic evidence for multi-generational mixing between Neolithic farmers and Mesolithic hunter–gatherers in the Lower Danube Basin. Curr. Biol. 27, 1801–1810.e10 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  49. 49

    Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50

    Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499–503 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51

    Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52

    Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  53. 53

    Wilde, S. et al. Direct evidence for positive selection of skin, hair, and eye pigmentation in Europeans during the last 5,000 y. Proc. Natl Acad. Sci. USA 111, 4832–4837 (2014). This study used ancient DNA data for alleles known to be involved in human pigmentation variation to identify a history of positive natural selection and estimate the strength of selection for each locus.

    CAS  Article  Google Scholar 

  54. 54

    Jeong, C. et al. Long-term genetic stability and a high-altitude East Asian origin for the peoples of the high valleys of the Himalayan arc. Proc. Natl Acad. Sci. USA 113, 7485–7490 (2016). This is an ancient genome study of eight individuals from Nepal (3,150–1,250 years BP ) that found staggered appearances and frequency increases for several genetic variants known from studies of modern regional populations to be associated with physiological adaptation to high altitude.

    CAS  Article  Google Scholar 

  55. 55

    Lorenzo, F. R. et al. A genetic mechanism for Tibetan high-altitude adaptation. Nat. Genet. 46, 951–956 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56

    Peng, Y. et al. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol. Biol. Evol. 28, 1075–1081 (2011).

    CAS  Article  Google Scholar 

  57. 57

    Ralph, P. & Coop, G. Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186, 647–668 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  58. 58

    Novembre, J., Galvani, A. P. & Slatkin, M. The geographic spread of the CCR5 Δ32 HIV-resistance allele. PLoS Biol. 3, e339 (2005).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  59. 59

    Richards, M. P., Schulting, R. J. & Hedges, R. E. M. Archaeology: sharp shift in diet at onset of Neolithic. Nature 425, 366–366 (2003).

    CAS  Article  Google Scholar 

  60. 60

    Chaplin, G. & Jablonski, N. G. The human environment and the vitamin D compromise: Scotland as a case study in human biocultural adaptation and disease susceptibility. Hum. Biol. 85, 529–552 (2013).

    Article  Google Scholar 

  61. 61

    Druzhkova, A. S. et al. Ancient DNA analysis affirms the canid from Altai as a primitive dog. PLoS ONE 8, e57754 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  62. 62

    Snir, A. et al. The origin of cultivation and proto-weeds, long before Neolithic farming. PLoS ONE 10, e0131422 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  63. 63

    Boivin, N. L. et al. Ecological consequences of human niche construction: examining long-term anthropogenic shaping of global species distributions. Proc. Natl Acad. Sci. USA 113, 6388–6396 (2016).

    CAS  Article  Google Scholar 

  64. 64

    Copeland, L., Blazek, J., Salman, H. & Tang, M. C. Form and functionality of starch. Food Hydrocoll. 23, 1527–1534 (2009).

    CAS  Article  Google Scholar 

  65. 65

    Gerbault, P. et al. Evolution of lactase persistence: an example of human niche construction. Phil. Trans. R. Soc. B. 366, 863–877 (2011).

    CAS  Article  Google Scholar 

  66. 66

    Campbell, A. K., Waud, J. P. & Matthews, S. B. The molecular basis of lactose intolerance. Sci. Prog. 88, 157–202 (2005).

    CAS  Article  Google Scholar 

  67. 67

    Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39, 31–40 (2007).

    CAS  Article  Google Scholar 

  68. 68

    Itan, Y., Powell, A., Beaumont, M. A., Burger, J. & Thomas, M. G. The origins of lactase persistence in Europe. PLoS Comput. Biol. 5, e1000491 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  69. 69

    Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886–6891 (2016).

    Article  CAS  Google Scholar 

  70. 70

    Burger, J., Kirchner, M., Bramanti, B., Haak, W. & Thomas, M. G. Absence of the lactase-persistence-associated allele in early Neolithic Europeans. Proc. Natl Acad. Sci. USA 104, 3736–3741 (2007). This was the first ancient DNA-based study of the history of the European lactase persistence allele; this study reported that the allele was not present in eight early Neolithic individuals (!7,500 years BP ) from four geographic sites, suggesting that the ability of individuals to digest lactose across their lifetimes likely post-dated the origin and spread of European dairying practices.

    CAS  Article  Google Scholar 

  71. 71

    Craig, O. E. et al. Did the first farmers of central and eastern Europe produce dairy foods? Antiquity 79, 882–894 (2005).

    Article  Google Scholar 

  72. 72

    Copley, M. S. et al. Direct chemical evidence for widespread dairying in prehistoric Britain. Proc. Natl Acad. Sci. USA 100, 1524–1529 (2003).

    CAS  Article  Google Scholar 

  73. 73

    Treuil, R. Dikili Tash, village préhistorique de Macédoine orientale. 1, Fouilles de Jean Deshayes (1961–1975), vol. 2, Bulletin de Correspondance Hellénique Supplément 37 (Ecole française d'Athènes, 2004).

    Google Scholar 

  74. 74

    Salque, M. et al. Earliest evidence for cheese making in the sixth millennium BC in northern Europe. Nature 493, 522–525 (2013).

    CAS  Article  Google Scholar 

  75. 75

    Perry, G. H. et al. Diet and the evolution of human amylase gene copy number variation. Nat. Genet. 39, 1256–1260 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  76. 76

    Inchley, C. E. et al. Selective sweep on human amylase genes postdates the split with Neanderthals. Sci. Rep. 6, 37198 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. 77

    Perry, G. H., Kistler, L., Kelaita, M. A. & Sams, A. J. Insights into hominin phenotypic and dietary evolution from ancient DNA sequence data. J. Hum. Evol. 79, 55–63 (2015).

    Article  Google Scholar 

  78. 78

    Mathias, R. A. et al. Adaptive evolution of the FADS gene cluster within Africa. PLoS ONE 7, e44926 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. 79

    Paul, B. D. & Snyder, S. H. The unusual amino acid l-ergothioneine is a physiologic cytoprotectant. Cell Death Differ. 17, 1134–1140 (2010).

    CAS  Article  Google Scholar 

  80. 80

    Huff, C. D. et al. Crohn's disease and genetic hitchhiking at IBD5. Mol. Biol. Evol. 29, 101–111 (2012).

    CAS  Article  Google Scholar 

  81. 81

    Lindo, J. et al. A time transect of exomes from a Native American population before and after European contact. Nat. Commun. 7, 13175 (2016). In this paper, the authors sequenced the exomes of 25 ancient First Nations individuals (!6,200–800 years BP ) from British Columbia, Canada, to identify an HLA-DQA1 gene haplotype with a substantial frequency difference compared with the Tsimshian descendant population living in the region today, potentially reflecting adaptation to disease outbreaks associated with European colonization (which post-dated the ancient DNA time series).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  82. 82

    Harkins, K. M. & Stone, A. C. Ancient pathogen genomics: insights into timing and adaptation. J. Hum. Evol. 79, 137–149 (2015).

    Article  Google Scholar 

  83. 83

    Bos, K. I. et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  84. 84

    Roffey, S. et al. Investigation of a medieval pilgrim burial excavated from the leprosarium of St Mary Magdalen Winchester. PLoS Negl. Trop. Dis. 11, e0005186 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  85. 85

    Spyrou, M. A. et al. Historical Y. pestis genomes reveal the European Black Death as the source of ancient and modern plague pandemics. Cell Host Microbe 19, 874–881 (2016).

    CAS  Article  Google Scholar 

  86. 86

    Marciniak, S. et al. Plasmodium falciparum malaria in 1 st−2nd century CE southern Italy. Curr. Biol. 26, R1220–R1222 (2016).

    CAS  Article  Google Scholar 

  87. 87

    Gelabert, P. et al. Mitochondrial DNA from the eradicated European Plasmodium vivax and P. falciparum from 70-year-old slides from the Ebro Delta in Spain. Proc. Natl Acad. Sci. USA 113, 11495–11500 (2016).

    CAS  Article  Google Scholar 

  88. 88

    Duggan, A. T. et al. 17 th century Variola virus reveals the recent history of smallpox. Curr. Biol. 26, 3407–3412 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  89. 89

    Devault, A. M. et al. Second-pandemic strain of Vibrio cholerae from the Philadelphia cholera outbreak of 1849. N. Engl. J. Med. 370, 334–340 (2014).

    CAS  Article  Google Scholar 

  90. 90

    Devault, A. M. et al. A molecular portrait of maternal sepsis from Byzantine Troy. eLife 6, e20983 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  91. 91

    Warinner, C. et al. Pathogens and host immunity in the ancient human oral cavity. Nat. Genet. 46, 336–344 (2014). This study reported ancient DNA results from dental calculus collected from four European individuals (!1,000–750 years BP ), including documentation of the presence of various pathogenic bacteria and producing direct evidence that pig, sheep, wheat and cruciferous vegetables were consumed as part of the diet.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  92. 92

    Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571–582 (2015). This paper sequenced seven Eurasian plague ( Yersinia pestis ) ancient genomes (!5,000–2,800 years BP ) and, among other findings, discovered that a gene encoding a protein necessary for Y. pestis viability in the flea gut was absent from genomes prior to !3,600 years BP ; the subsequent acquisition of this gene through horizontal transfer likely helped facilitate the bubonic plague transmission cycle.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. 93

    Hinnebusch, B. J. et al. Role of Yersinia murine toxin in survival of Yersinia pestis in the midgut of the flea vector. Science 296, 733–735 (2002).

    CAS  Article  Google Scholar 

  94. 94

    Bos, K. I. et al. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506–510 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. 95

    Hummel, S., Schmidt, D., Kremeyer, B., Herrmann, B. & Oppermann, M. Detection of the CCR5-Δ32 HIV resistance gene in Bronze Age skeletons. Genes Immun. 6, 371–374 (2005).

    CAS  Article  Google Scholar 

  96. 96

    Wolpoff, M. H., Thorne, A. G., Smith, F. H., Frayer, D. W. & Pope, G. G. in Origins of Anatomically Modern Humans (eds Nitecki, M. H. & Nitecki, D.) V.) 175–199 (Plenum Press, 1994).

    Book  Google Scholar 

  97. 97

    Tattersall, I. Out of Africa: modern human origins special feature: human origins: out of Africa. Proc. Natl Acad. Sci. USA 106, 16018–16021 (2009).

    CAS  Article  Google Scholar 

  98. 98

    Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710–722 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. 99

    Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053–1060 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. 100

    Vernot, B. & Akey, J. M. Resurrecting surviving Neandertal lineages from modern human genomes. Science 343, 1017–1021 (2014).

    CAS  Article  Google Scholar 

  101. 101

    Dannemann, M., Prüfer, K. & Kelso, J. Functional implications of Neandertal introgression in modern humans. Genome Biol. 18, 61–72 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  102. 102

    Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43–49 (2014).

    Article  CAS  Google Scholar 

  103. 103

    Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 104

    Huerta-Sánchez, E. et al. Altitude adaptation in Tibet caused by introgression of Denisovan-like DNA. Nature 512, 194–197 (2014). This paper demonstrated that a genetic haplotype surrounding the EPAS1 gene that underlies a physiological adaptation to high altitude in modern Tibetans is the result of adaptive introgression from Denisovans or a related archaic hominin population.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  105. 105

    Racimo, F. et al. Archaic adaptive introgression in TBX15/WARS2. Mol. Biol. Evol. 34, 509–524 (2017).

    CAS  Google Scholar 

  106. 106

    Skoglund, P. & Jakobsson, M. Archaic human ancestry in East Asia. Proc. Natl Acad. Sci. USA 108, 18301–18306 (2011).

    CAS  Article  Google Scholar 

  107. 107

    Reich, D. et al. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am. J. Hum. Genet. 89, 516–528 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  108. 108

    Castellano, S. et al. Patterns of coding variation in the complete exomes of three Neandertals. Proc. Natl Acad. Sci. USA 111, 6666–6671 (2014).

    CAS  Article  Google Scholar 

  109. 109

    Lalueza-Fox, C. et al. A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science 318, 1453–1455 (2007).

    CAS  Article  Google Scholar 

  110. 110

    Lalueza-Fox, C., Gigli, E., de la Rasilla, M., Fortea, J. & Rosas, A. Bitter taste perception in Neanderthals through the analysis of the TAS2R38 gene. Biol. Lett. 5, 809–811 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  111. 111

    McCoy, R. C., Wakefield, J. & Akey, J. M. Impacts of Neanderthal-introgressed sequences on the landscape of human gene expression. Cell 168, 916–927 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. 112

    Simonti, C. N. et al. The phenotypic legacy of admixture between modern humans and Neandertals. Science 351, 737–741 (2016). This study used electronic health record phenotypes from a large sample of modern human patients to associate alleles originally introgressed from Neandertals with increased risk of depression, skin lesions associated with sun exposure (actinic keratosis), and other phenotypes.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  113. 113

    Gittelman, R. M. et al. Archaic hominin admixture facilitated adaptation to Out-of-Africa environments. Curr. Biol. 26, 3375–3382 (2016). This paper analysed 126 genomic regions containing strong signatures of adaptive introgression from archaic hominins identified in a sample of geographically diverse human populations; these loci are significantly enriched for genes involved in the immune response and also contain multiple genes with known roles in skin pigmentation.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. 114

    Racimo, F., Sankararaman, S., Nielsen, R. & Huerta-Sánchez, E. Evidence for archaic adaptive introgression in humans. Nat. Rev. Genet. 16, 359–371 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. 115

    Sankararaman, S. et al. The landscape of Neandertal ancestry in present-day humans. Nature 507, 354–357 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. 116

    Vernot, B. et al. Excavating Neandertal and Denisovan DNA from the genomes of Melanesian individuals. Science 352, 235–239 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  117. 117

    Fumagalli, M. et al. Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349, 1343–1347 (2015).

    CAS  Article  Google Scholar 

  118. 118

    Gburcik, V., Cawthorn, W. P., Nedergaard, J., Timmons, J. A. & Cannon, B. An essential role for Tbx15 in the differentiation of brown and 'brite' but not white adipocytes. Am. J. Physiol. Endocrinol. Metab. 303, E1053–E1060 (2012).

    CAS  Article  Google Scholar 

  119. 119

    Deschamps, M. et al. Genomic signatures of selective pressures and introgression from archaic hominins at human innate immunity genes. Am. J. Hum. Genet. 98, 5–21 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  120. 120

    Enard, D. & Petrov, D. A. RNA viruses drove adaptive introgressions between Neanderthals and modern humans. Preprint at bioRxiv (2017).

  121. 121

    Abi-Rached, L. et al. The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334, 89–94 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. 122

    Sams, A. J. et al. Adaptively introgressed Neandertal haplotype at the OAS locus functionally impacts innate immune responses in humans. Genome Biol. 17, 246–261 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  123. 123

    Sullivan, A. P., de Manuel, M., Marques-Bonet, T. & Perry, G. H. An evolutionary medicine perspective on Neandertal extinction. J. Hum. Evol. 108, 62–71 (2017).

    Article  Google Scholar 

  124. 124

    Houldcroft, C. J. & Underdown, S. J. Neanderthal genomics suggests a pleistocene time frame for the first epidemiologic transition. Am. J. Phys. Anthropol. 160, 379–388 (2016).

    Article  Google Scholar 

  125. 125

    Key, F. M., Teixeira, J. C., de Filippo, C. & Andrés, A. M. Advantageous diversity maintained by balancing selection in humans. Curr. Opin. Genet. Dev. 29, 45–51 (2014).

    CAS  Article  Google Scholar 

  126. 126

    Nédélec, Y. et al. Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell 167, 657–669 (2016).

    Article  CAS  Google Scholar 

  127. 127

    Quach, H. et al. Genetic adaptation and Neandertal admixture shaped the immune system of human populations. Cell 167, 643–656.e17 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  128. 128

    Park, S. D. E. et al. Genome sequencing of the extinct Eurasian wild aurochs, Bos primigenius, illuminates the phylogeography and evolution of cattle. Genome Biol. 16, 234–249 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. 129

    Loog, L. et al. Inferring allele frequency trajectories from ancient DNA indicates that selection on a chicken gene coincided with changes in medieval husbandry practices. Mol. Biol. Evol. (2017). This study of domestic chickens connected the ancient DNA-informed timing of a significant change in frequency for an allele associated with increased egg production to concomitant increases in the intensity of chicken husbandry as documented by historical and archaeological records.

  130. 130

    MacHugh, D. E., Larson, G. & Orlando, L. Taming the past: ancient DNA and the study of animal domestication. Annu. Rev. Anim. Biosci. 5, 329–351 (2017).

    CAS  Article  Google Scholar 

  131. 131

    Ramos-Madrigal, J. et al. Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Curr. Biol. 26, 3195–3201 (2016). This study identified a mix of ancestral and derived functional genetic variants in maize from Mexico !5,300 years BP , highlighting the gradual temporal process of trait evolution in this domestic species.

    CAS  Article  Google Scholar 

  132. 132

    Schubert, M. et al. Prehistoric genomes reveal the genetic foundation and cost of horse domestication. Proc. Natl Acad. Sci. USA 111, E5661–E5669 (2014).

    CAS  Article  Google Scholar 

  133. 133

    Ollivier, M. et al. Amy2B copy number variation reveals starch diet adaptations in ancient European dogs. R. Soc. Open Sci. 3, 160449 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  134. 134

    Librado, P. et al. Tracking the origins of Yakutian horses and the genetic basis for their fast adaptation to subarctic environments. Proc. Natl Acad. Sci. USA 112, E6889–E6897 (2015).

    CAS  Article  Google Scholar 

  135. 135

    Jaenicke-Després, V. et al. Early allelic selection in maize as revealed by ancient DNA. Science 302, 1206–1208 (2003).

    Article  CAS  Google Scholar 

  136. 136

    Flink, L. G. et al. Establishing the validity of domestication genes using DNA from ancient chickens. Proc. Natl Acad. Sci. USA 111, 6184–6189 (2013).

    Article  CAS  Google Scholar 

  137. 137

    West, B. & Zhou, B.-X. Did chickens go North? New evidence for domestication. J. Archaeol. Sci. 15, 515–533 (1988).

    Article  Google Scholar 

  138. 138

    Librado, P. et al. Ancient genomic changes associated with domestication of the horse. Science 356, 442–445 (2017).

    CAS  Article  Google Scholar 

  139. 139

    Outram, A. K. et al. The earliest horse harnessing and milking. Science 323, 1332–1335 (2009).

    CAS  Article  Google Scholar 

  140. 140

    Ludwig, A. et al. Coat colour variation at the beginning of horse domestication. Science 324, 485 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  141. 141

    Ludwig, A. et al. Twenty-five thousand years of fluctuating selection on leopard complex spotting and congenital night blindness in horses. Phil. Trans. R. Soc. B. 370, 20130386 (2014).

    Article  CAS  Google Scholar 

  142. 142

    Ottoni, C. et al. The palaeogenetics of cat dispersal in the ancient world. Nat. Ecol. Evol. 1, 0139 (2017).

    Article  Google Scholar 

  143. 143

    Axelsson, E. et al. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495, 360–364 (2013).

    CAS  Article  Google Scholar 

  144. 144

    Arendt, M., Cairns, K. M., Ballard, J. W. O., Savolainen, P. & Axelsson, E. Diet adaptation in dog reflects spread of prehistoric agriculture. Heredity 117, 301–306 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. 145

    Botigué, L. R. et al. Ancient European dog genomes reveal continuity since the Early Neolithic. Nat. Commun. 8, 16082 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  146. 146

    Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352, 1228–1231 (2016).

    CAS  Article  Google Scholar 

  147. 147

    Kistler, L., Ware, R., Smith, O., Collins, M. & Allaby, R. G. A new model for ancient DNA decay based on paleogenomic meta-analysis. Nucleic Acids Res. 45, 6310–6320 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  148. 148

    Fehren-Schmitz, L. & Georges, L. Ancient DNA reveals selection acting on genes associated with hypoxia response in pre-Columbian Peruvian Highlanders in the last 8500 years. Sci. Rep. 6, 23485 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  149. 149

    Sullivan, A. P., Bird, D. W. & Perry, G. H. Human behaviour as a long-term ecological driver of non-human evolution. Nat. Ecol. Evol. 1, 0065 (2017).

    Article  Google Scholar 

  150. 150

    Noonan, J. P. et al. Sequencing and analysis of Neanderthal genomic DNA. Science 314, 1113–1118 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  151. 151

    Green, R. E. et al. Analysis of one million base pairs of Neanderthal DNA. Nature 444, 330–336 (2006).

    CAS  Article  Google Scholar 

  152. 152

    Ramírez, O. et al. Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean Caprine. PLoS ONE 4, e5670 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  153. 153

    Miller, W. et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 456, 387–390 (2008).

    CAS  Article  Google Scholar 

  154. 154

    Lambert, D. M. & Millar, C. D. Evolutionary biology: ancient genomics is born. Nature 444, 275–276 (2006).

    CAS  Article  Google Scholar 

  155. 155

    Wall, J. D. & Kim, S. K. Inconsistencies in Neanderthal genomic DNA sequences. PLoS Genet. 3, 1862–1866 (2007).

    CAS  Article  Google Scholar 

  156. 156

    Rasmussen, M. et al. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463, 757–762 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  157. 157

    Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  158. 158

    Pinhasi, R. et al. Optimal ancient DNA yields from the inner ear part of the human petrous bone. PLoS ONE 10, e0129102 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  159. 159

    Gansauge, M.-T. & Meyer, M. Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat. Protoc. 8, 737–748 (2013).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  160. 160

    Carpenter, M. L. et al. Pulling out the 1%: whole-genome capture for the targeted enrichment of ancient DNA sequencing libraries. Am. J. Hum. Genet. 93, 852–864 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  161. 161

    Hofreiter, M. et al. The future of ancient DNA: technical advances and conceptual shifts. BioEssays 37, 284–293 (2015).

    Article  Google Scholar 

  162. 162

    Gron, K. J. et al. Cattle management for dairying in Scandinavia's earliest Neolithic. PLoS ONE 10, e0131267 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  163. 163

    Zeder, M. A. & Hesse, B. The initial domestication of goats (Capra hircus) in the Zagros mountains 10,000 years ago. Science 287, 2254–2257 (2000).

    CAS  Article  Google Scholar 

  164. 164

    Cramp, L. J. E. et al. Neolithic dairy farming at the extreme of agriculture in northern Europe. Proc. Biol. Sci. 281, 20140819 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  165. 165

    Warinner, C. et al. Direct evidence of milk consumption from ancient human dental calculus. Sci. Rep. 4, 7104 (2015).

    Article  CAS  Google Scholar 

  166. 166

    Yang, Y. et al. Proteomics evidence for kefir dairy in Early Bronze Age China. J. Archaeol. Sci. 45, 178–186 (2014).

    CAS  Article  Google Scholar 

  167. 167

    Burbano, H. A. et al. Targeted investigation of the Neandertal genome by array-based sequence capture. Science 328, 723–725 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  168. 168

    Rasmussen, M. et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94–98 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  169. 169

    Keller, A. et al. New insights into the Tyrolean Iceman's origin and phenotype as inferred by whole-genome sequencing. Nat. Commun. 3, 698 (2012).

    Article  CAS  Google Scholar 

  170. 170

    Skoglund, P. et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336, 466–469 (2012).

    CAS  Article  Google Scholar 

  171. 171

    Fu, Q. et al. DNA analysis of an early modern human from Tianyuan Cave, China. Proc. Natl Acad. Sci. USA 110, 2223–2227 (2013).

    CAS  Article  Google Scholar 

  172. 172

    Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  173. 173

    Schroeder, H. et al. Genome-wide ancestry of 17 th-century enslaved Africans from the Caribbean. Proc. Natl Acad. Sci. USA 112, 3669–3673 (2015).

    CAS  Article  Google Scholar 

  174. 174

    Malaspinas, A.-S. et al. Two ancient human genomes reveal Polynesian ancestry among the indigenous Botocudos of Brazil. Curr. Biol. 24, R1035–R1037 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  175. 175

    Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87–91 (2014).

    Article  CAS  Google Scholar 

  176. 176

    Rasmussen, M. et al. The genome of a Late Pleistocene human from a Clovis burial site in western Montana. Nature 506, 225–229 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  177. 177

    Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014).

    CAS  Article  Google Scholar 

  178. 178

    Skoglund, P. et al. Genomic diversity and admixture differs for Stone-Age Scandinavian foragers and farmers. Science 344, 747–750 (2014).

    CAS  Article  Google Scholar 

  179. 179

    Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216–219 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  180. 180

    Gallego Llorente, M. et al. Ancient Ethiopian genome reveals extensive Eurasian admixture in Eastern Africa. Science 350, 820–822 (2015).

    CAS  Article  Google Scholar 

  181. 181

    Olalde, I. et al. A common genetic origin for early farmers from Mediterranean Cardial and Central European LBK cultures. Mol. Biol. Evol. 32, 3132–3142 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. 182

    Raghavan, M. et al. Genomic evidence for the Pleistocene and recent population history of Native Americans. Science 349, aab3884 (2015).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  183. 183

    Sawyer, S. et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals. Proc. Natl Acad. Sci. USA 112, 15696–15700 (2015).

    CAS  Article  Google Scholar 

  184. 184

    Rasmussen, M. et al. The ancestry and affiliations of Kennewick Man. Nature 523, 455–458 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  185. 185

    Martiniano, R. et al. Genomic signals of migration and continuity in Britain before the Anglo-Saxons. Nat. Commun. 7, 10326 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  186. 186

    Schiffels, S. et al. Iron Age and Anglo-Saxon genomes from East England reveal British migration history. Nat. Commun. 7, 10408 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  187. 187

    Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  188. 188

    Gallego Llorente, M. et al. The genetics of an early Neolithic pastoralist from the Zagros, Iran. Sci. Rep. 6, 31326 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  189. 189

    Kılınç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659–2666 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  190. 190

    Omrak, A. et al. Genomic evidence establishes Anatolia as the source of the European Neolithic gene pool. Curr. Biol. 26, 270–275 (2016).

    CAS  Article  Google Scholar 

  191. 191

    Meyer, M. et al. Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature 531, 504–507 (2016).

    CAS  Article  Google Scholar 

  192. 192

    Skoglund, P. et al. Genomic insights into the peopling of the Southwest Pacific. Nature 538, 510–513 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  193. 193

    Jones, E. R. et al. The Neolithic transition in the Baltic was not driven by admixture with early European farmers. Curr. Biol. 27, 576–582 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  194. 194

    Unterländer, M. et al. Ancestry and demography and descendants of Iron Age nomads of the Eurasian Steppe. Nat. Commun. 8, 14615 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  195. 195

    Lipson, M. et al. Parallel ancient genomic transects reveal complex population history of early European farmers. Preprint at bioRxiv (2017).

  196. 196

    Lindo, J. et al. Ancient individuals from the North American Northwest Coast reveal 10,000 years of regional genetic continuity. Proc. Natl Acad. Sci. USA 114, 4093–4098 (2017).

    CAS  Article  Google Scholar 

  197. 197

    Kennett, D. J. et al. Archaeogenomic evidence reveals prehistoric matrilineal dynasty. Nat. Commun. 8, 14115 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  198. 198

    Mathieson, I. et al. The genomic history of southeastern Europe. Preprint at bioRxiv (2017).

  199. 199

    Martiniano, R. et al. The population genomics of archaeological transition in west Iberia: Investigation of ancient substructure using imputation and haplotype-based methods. PLoS Genet. 13, e1006852 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  200. 200

    Siska, V. et al. Genome-wide data from two early Neolithic East Asian individuals dating to 7700 years ago. Sci. Adv. 3, e1601877 (2017).

    PubMed  PubMed Central  Article  Google Scholar 

  201. 201

    Haber, M. et al. Continuity and admixture in the last five millennia of Levantine history from ancient Canaanite and present-day Lebanese genome sequences. Am. J. Hum. Genet. (2017).

  202. 202

    Schuenemann, V. J. et al. Ancient Egyptian mummy genomes suggest an increase of Sub-Saharan African ancestry in post-Roman periods. Nat. Commun. 8, 15694 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  203. 203

    Schlebusch, C. M. et al. Ancient genomes from southern Africa pushes modern human divergence beyond 260,000 years ago. Preprint at bioRxiv (2017).

  204. 204

    Mittnik, A. et al. The genetic history of northern Europe. Preprint at bioRxiv (2017).

  205. 205

    Slon, V. et al. A fourth Denisovan individual. Sci. Adv. 3, e1700186 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  206. 206

    Kuhlwilm, M. et al. Ancient gene flow from early modern humans into Eastern Neanderthals. Nature 530, 429–433 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references


The authors thank C. Bergey and R. George for discussion about the manuscript. This work was supported by grants from the National Science Foundation (BCS-1554834 and BCS-1317163; to G.H.P.).

Author information




The authors contributed equally to all aspects of this manuscript.

Corresponding author

Correspondence to George H. Perry.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information S1 (table)

Spatiotemporal frequencies of the European lactase persistence allele. (PDF 186 kb)

PowerPoint slides



A process of phenotypic and corresponding genetic change over time for traits that confer increased reproductive fitness in a given environmental context.

Positive natural selection

A mechanism of evolution in which a genetically mediated trait that confers a relative fitness advantage increases in frequency over time because of that advantage. In this Review, we refer to positive selection as an adaptive process that can act on new or previously existing genetic variants.


Physical traits of an organism; often refers to externally visible traits but may include internal and microscopic or biochemical traits.

Ancient DNA

DNA from palaeontological, archaeological, or historical but pre-modern biological specimens that is often damaged and degraded and recovered in small quantities.


All or nearly all protein-coding gene regions of the nuclear genome; in humans, representing approximately 1% of the genome.

Single-nucleotide polymorphism

(SNP). A single position in the reference genome at which the specific nucleotide present (thymine, guanine, cytosine, or adenine) varies among individuals in a population or species.

Archaic hominins

Now-extinct populations or species that are distinct from anatomically modern humans but that share a more recent common ancestor with modern humans than with chimpanzees — for example, Neandertals and Denisovans.

Anatomically modern humans

Hominins recognizable phenotypically as early members of our own species, Homo sapiens, first appearing >200,000 years BP in Africa.

Adaptive introgression

The process of a genetic variant that was originally introduced into a population via admixture increasing in frequency by positive natural selection because it confers a fitness advantage.

Genetic drift

Changes in genetic variation over time that are due to random (chance) processes, apart from natural selection.

Gene flow

Movement of genetic variation between populations, for example, through migration or admixture.


A cultural period in human prehistory characterized by early technological and demographic shifts associated with the transition to farming and pastoralism, occurring at different times across regions.


A process of plant and animal evolution mediated by human selection for particular phenotypes (artificial selection), sometimes combined with commensal adaptation to human-constructed niches.

Biocultural adaptation

The process of interaction between human cultural and adaptive biological change (for example, dairying and the ability of adults to digest milk sugars).


The ability of a pathogen to be directly or indirectly transmitted to humans from animals sharing the same habitat.


Interbreeding between previously isolated populations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marciniak, S., Perry, G. Harnessing ancient genomes to study the history of human adaptation. Nat Rev Genet 18, 659–674 (2017).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing