Harnessing ancient genomes to study the history of human adaptation

Nature Reviews Genetics

Volumn 18, Issue 11, 2017, Pages 659-674

  Marciniak, Stephanie ^a   Perry, George H ^a,b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANCIENT DNA;

ADAPTATION; DOMESTICATION; EVOLUTION; EVOLUTIONARY ADAPTATION; GENETIC VARIABILITY; GENOME; HUMAN; INFECTIOUS AGENT; INTROGRESSION; LIFESTYLE; PRIORITY JOURNAL; REVIEW; ANIMAL; GENETICS; HOMO NEANDERTHALENSIS; HUMAN GENOME;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; GENOME, HUMAN; HUMANS; NEANDERTHALS;

EID: 85031732314     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg.2017.65     Document Type: Review

References (206)

1. Huxley, T. H. Evidence as to Man's Place in Nature (Williams and Norgate, 1863).
2. Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871).
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).
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).
5. Scheinfeldt, L. B. & Tishkoff, S. A. Recent human adaptation: genomic approaches, interpretation and insights. Nat. Rev. Genet. 14, 692-702 (2013).
6. Sabeti, P. C. et al. Positive natural selection in the human lineage. Science 312, 1614-1620 (2006).
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).
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).
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).
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).
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).
12. Nielsen, R. et al. Tracing the peopling of the world through genomics. Nature 541, 302-310 (2017).
13. Orlando, L., Gilbert, M. T. P. & Willerslev, E. Reconstructing ancient genomes and epigenomes. Nat. Rev. Genet. 16, 395-408 (2015).
14. Llamas, B., Willerslev, E. & Orlando, L. Human evolution: a tale from ancient genomes. Phil. Trans. R. Soc. B 372, 20150484 (2016).
15. Nakagome, S. et al. Estimating the ages of selection signals from different epochs in human history. Mol. Biol. Evol. 33, 657-669 (2016).
16. Field, Y. et al. Detection of human adaptation during the past 2000 years. Science 354, 760-764 (2016).
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).
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).
19. Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).
20. Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499-503 (2015).
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).
22. Buckley, M. T. et al. Selection in Europeans on fatty acid desaturases associated with dietary changes. Mol. Biol. Evol. 34, 1307-1318 (2017).
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).
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).
25. Günther, T. et al. Genomics of Mesolithic Scandinavia reveal colonization routes and high-latitude adaptation. Preprint at bioRxiv http://dx.doi. org/10.1101/164400 (2017).
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).
27. Allentoft, M. E. et al. Population genomics of Bronze Age Eurasia. Nature 522, 167-172 (2015).
28. Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207-211 (2015).
29. Olalde, I. et al. The Beaker phenomenon and the genomic transformation of northwest Europe. Preprint at bioRxiv http://dx.doi.org/10.1101/135962 (2017).
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).
31. Shennan, S. Evolutionary demography and the population history of the European early Neolithic. Hum. Biol. 81, 339-355 (2009).
32. Leonardi, M. et al. Evolutionary patterns and processes: lessons from ancient DNA. Syst. Biol. 66, e1-e29 (2017).
33. Mirazón Lahr, M. The shaping of human diversity: filters, boundaries and transitions. Phil. Trans. R. Soc. B 371, http://dx.doi.org/10.1098/rstb.2015.0241 (2016).
34. Stewart, J. R. & Stringer, C. B. Human evolution out of Africa: the role of refugia and climate change. Science 335, 1317-1321 (2012).
35. Richards, M. A brief review of the archaeological evidence for Palaeolithic and Neolithic subsistence. Eur. J. Clin. Nutr. 56, 1262-1278 (2002).
36. Perry, G. H. Parasites and human evolution. Evol. Anthropol. 23, 218-228 (2014).
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).
38. Jablonski, N. G. & Chaplin, G. Human skin pigmentation as an adaptation to UV radiation. Proc. Natl Acad. Sci. USA 107, 8962-8968 (2010).
39. Chaplin, G. & Jablonski, N. G. Vitamin D and the evolution of human depigmentation. Am. J. Phys. Anthropol. 139, 451-461 (2009).
40. Brickley, M. B. et al. Ancient vitamin D deficiency: long-term trends. Curr. Anthropol. 58, 420-427 (2017).
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).
42. Bodnar, L. M. et al. Maternal vitamin D deficiency increases the risk of preeclampsia. J. Clin. Endocrinol. Metab. 92, 3517-3522 (2007).
43. Wang, T. J. et al. Common genetic determinants of vitamin D insufficiency: a genome-wide association study. Lancet 376, 180-188 (2010).
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).
45. Sturm, R. A. et al. Human pigmentation genes under environmental selection. Genome Biol. 13, 248-263 (2012).
46. Beleza, S. et al. The timing of pigmentation lightening in Europeans. Mol. Biol. Evol. 30, 24-35 (2013).
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).
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).
49. Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 8912 (2015).
50. Broushaki, F. et al. Early Neolithic genomes from the eastern Fertile Crescent. Science 353, 499-503 (2016).
51. Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225-228 (2014).
52. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409-413 (2014).
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).
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).
55. Lorenzo, F. R. et al. A genetic mechanism for Tibetan high-altitude adaptation. Nat. Genet. 46, 951-956 (2014).
56. Peng, Y. et al. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol. Biol. Evol. 28, 1075-1081 (2011).
57. Ralph, P. & Coop, G. Parallel adaptation: one or many waves of advance of an advantageous allele? Genetics 186, 647-668 (2010).
58. Novembre, J., Galvani, A. P. & Slatkin, M. The geographic spread of the CCR5 Δ32 HIV-resistance allele. PLoS Biol. 3, e339 (2005).
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).
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).
61. Druzhkova, A. S. et al. Ancient DNA analysis affirms the canid from Altai as a primitive dog. PLoS ONE 8, e57754 (2013).
62. Snir, A. et al. The origin of cultivation and proto-weeds, long before Neolithic farming. PLoS ONE 10, e0131422 (2015).
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).
64. Copeland, L., Blazek, J., Salman, H. & Tang, M. C. Form and functionality of starch. Food Hydrocoll. 23, 1527-1534 (2009).
65. Gerbault, P. et al. Evolution of lactase persistence: an example of human niche construction. Phil. Trans. R. Soc. B. 366, 863-877 (2011).
66. Campbell, A. K., Waud, J. P. & Matthews, S. B. The molecular basis of lactose intolerance. Sci. Prog. 88, 157-202 (2005).
67. Tishkoff, S. A. et al. Convergent adaptation of human lactase persistence in Africa and Europe. Nat. Genet. 39, 31-40 (2007).
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).
69. Hofmanová, Z. et al. Early farmers from across Europe directly descended from Neolithic Aegeans. Proc. Natl Acad. Sci. USA 113, 6886-6891 (2016).
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).
71. Craig, O. E. et al. Did the first farmers of central and eastern Europe produce dairy foods? Antiquity 79, 882-894 (2005).
72. Copley, M. S. et al. Direct chemical evidence for widespread dairying in prehistoric Britain. Proc. Natl Acad. Sci. USA 100, 1524-1529 (2003).
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).
74. Salque, M. et al. Earliest evidence for cheese making in the sixth millennium BC in northern Europe. Nature 493, 522-525 (2013).
75. Perry, G. H. et al. Diet and the evolution of human amylase gene copy number variation. Nat. Genet. 39, 1256-1260 (2007).
76. Inchley, C. E. et al. Selective sweep on human amylase genes postdates the split with Neanderthals. Sci. Rep. 6, 37198 (2016).
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).
78. Mathias, R. A. et al. Adaptive evolution of the FADS gene cluster within Africa. PLoS ONE 7, e44926 (2012).
79. Paul, B. D. & Snyder, S. H. The unusual amino acid l-ergothioneine is a physiologic cytoprotectant. Cell Death Differ. 17, 1134-1140 (2010).
80. Huff, C. D. et al. Crohn's disease and genetic hitchhiking at IBD5. Mol. Biol. Evol. 29, 101-111 (2012).
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).
82. Harkins, K. M. & Stone, A. C. Ancient pathogen genomics: insights into timing and adaptation. J. Hum. Evol. 79, 137-149 (2015).
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).
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).
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).
86. Marciniak, S. et al. Plasmodium falciparum malaria in 1 st-2nd century CE southern Italy. Curr. Biol. 26, R1220-R1222 (2016).
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).
88. Duggan, A. T. et al. 17 th century Variola virus reveals the recent history of smallpox. Curr. Biol. 26, 3407-3412 (2016).
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).
90. Devault, A. M. et al. A molecular portrait of maternal sepsis from Byzantine Troy. eLife 6, e20983 (2017).
91. Warinner, C. et al. Pathogens and host immunity in the ancient human oral cavity. Nat. Genet. 46, 336-344 (2014).
92. Rasmussen, S. et al. Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163, 571-582 (2015).
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).
94. Bos, K. I. et al. A draft genome of Yersinia pestis from victims of the Black Death. Nature 478, 506-510 (2011).
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).
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).
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).
98. Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710-722 (2010).
99. Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053-1060 (2010).
100. Vernot, B. & Akey, J. M. Resurrecting surviving Neandertal lineages from modern human genomes. Science 343, 1017-1021 (2014).
101. Dannemann, M., Prüfer, K. & Kelso, J. Functional implications of Neandertal introgression in modern humans. Genome Biol. 18, 61-72 (2017).
102. Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43-49 (2014).
103. Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222-226 (2012).
104. Huerta-Sánchez, E. et al. Altitude adaptation in Tibet caused by introgression of Denisovan-like DNA. Nature 512, 194-197 (2014).
105. Racimo, F. et al. Archaic adaptive introgression in TBX15/WARS2. Mol. Biol. Evol. 34, 509-524 (2017).
106. Skoglund, P. & Jakobsson, M. Archaic human ancestry in East Asia. Proc. Natl Acad. Sci. USA 108, 18301-18306 (2011).
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).
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).
109. Lalueza-Fox, C. et al. A melanocortin 1 receptor allele suggests varying pigmentation among Neanderthals. Science 318, 1453-1455 (2007).
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).
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).
112. Simonti, C. N. et al. The phenotypic legacy of admixture between modern humans and Neandertals. Science 351, 737-741 (2016).
113. Gittelman, R. M. et al. Archaic hominin admixture facilitated adaptation to Out-of-Africa environments. Curr. Biol. 26, 3375-3382 (2016).
114. Racimo, F., Sankararaman, S., Nielsen, R. & Huerta-Sánchez, E. Evidence for archaic adaptive introgression in humans. Nat. Rev. Genet. 16, 359-371 (2015).
115. Sankararaman, S. et al. The landscape of Neandertal ancestry in present-day humans. Nature 507, 354-357 (2014).
116. Vernot, B. et al. Excavating Neandertal and Denisovan DNA from the genomes of Melanesian individuals. Science 352, 235-239 (2016).
117. Fumagalli, M. et al. Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349, 1343-1347 (2015).
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).
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).
120. Enard, D. & Petrov, D. A. RNA viruses drove adaptive introgressions between Neanderthals and modern humans. Preprint at bioRxiv http://dx.doi. org/10.1101/120477 (2017).
121. Abi-Rached, L. et al. The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334, 89-94 (2011).
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).
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).
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).
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).
126. Nédélec, Y. et al. Genetic ancestry and natural selection drive population differences in immune responses to pathogens. Cell 167, 657-669 (2016).
127. Quach, H. et al. Genetic adaptation and Neandertal admixture shaped the immune system of human populations. Cell 167, 643-656.e17 (2016).
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).
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. http://dx.doi.org/10.1093/molbev/msx142 (2017).
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).
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).
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).
133. Ollivier, M. et al. Amy2B copy number variation reveals starch diet adaptations in ancient European dogs. R. Soc. Open Sci. 3, 160449 (2016).
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).
135. Jaenicke-Després, V. et al. Early allelic selection in maize as revealed by ancient DNA. Science 302, 1206-1208 (2003).
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).
137. West, B. & Zhou, B.-X. Did chickens go North? New evidence for domestication. J. Archaeol. Sci. 15, 515-533 (1988).
138. Librado, P. et al. Ancient genomic changes associated with domestication of the horse. Science 356, 442-445 (2017).
139. Outram, A. K. et al. The earliest horse harnessing and milking. Science 323, 1332-1335 (2009).
140. Ludwig, A. et al. Coat colour variation at the beginning of horse domestication. Science 324, 485 (2009).
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).
142. Ottoni, C. et al. The palaeogenetics of cat dispersal in the ancient world. Nat. Ecol. Evol. 1, 0139 (2017).
143. Axelsson, E. et al. The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495, 360-364 (2013).
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).
145. Botigué, L. R. et al. Ancient European dog genomes reveal continuity since the Early Neolithic. Nat. Commun. 8, 16082 (2017).
146. Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352, 1228-1231 (2016).
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).
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).
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).
150. Noonan, J. P. et al. Sequencing and analysis of Neanderthal genomic DNA. Science 314, 1113-1118 (2006).
151. Green, R. E. et al. Analysis of one million base pairs of Neanderthal DNA. Nature 444, 330-336 (2006).
152. Ramírez, O. et al. Paleogenomics in a temperate environment: shotgun sequencing from an extinct Mediterranean Caprine. PLoS ONE 4, e5670 (2009).
153. Miller, W. et al. Sequencing the nuclear genome of the extinct woolly mammoth. Nature 456, 387-390 (2008).
154. Lambert, D. M. & Millar, C. D. Evolutionary biology: ancient genomics is born. Nature 444, 275-276 (2006).
155. Wall, J. D. & Kim, S. K. Inconsistencies in Neanderthal genomic DNA sequences. PLoS Genet. 3, 1862-1866 (2007).
156. Rasmussen, M. et al. Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463, 757-762 (2010).
157. Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419-424 (2016).
158. Pinhasi, R. et al. Optimal ancient DNA yields from the inner ear part of the human petrous bone. PLoS ONE 10, e0129102 (2015).
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).
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).
161. Hofreiter, M. et al. The future of ancient DNA: technical advances and conceptual shifts. BioEssays 37, 284-293 (2015).
162. Gron, K. J. et al. Cattle management for dairying in Scandinavia's earliest Neolithic. PLoS ONE 10, e0131267 (2015).
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).
164. Cramp, L. J. E. et al. Neolithic dairy farming at the extreme of agriculture in northern Europe. Proc. Biol. Sci. 281, 20140819 (2014).
165. Warinner, C. et al. Direct evidence of milk consumption from ancient human dental calculus. Sci. Rep. 4, 7104 (2015).
166. Yang, Y. et al. Proteomics evidence for kefir dairy in Early Bronze Age China. J. Archaeol. Sci. 45, 178-186 (2014).
167. Burbano, H. A. et al. Targeted investigation of the Neandertal genome by array-based sequence capture. Science 328, 723-725 (2010).
168. Rasmussen, M. et al. An Aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94-98 (2011).
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).
170. Skoglund, P. et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science 336, 466-469 (2012).
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).
172. Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445-449 (2014).
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).
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).
175. Raghavan, M. et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature 505, 87-91 (2014).
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).
177. Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113-1118 (2014).
178. Skoglund, P. et al. Genomic diversity and admixture differs for Stone-Age Scandinavian foragers and farmers. Science 344, 747-750 (2014).
179. Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216-219 (2015).
180. Gallego Llorente, M. et al. Ancient Ethiopian genome reveals extensive Eurasian admixture in Eastern Africa. Science 350, 820-822 (2015).
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).
182. Raghavan, M. et al. Genomic evidence for the Pleistocene and recent population history of Native Americans. Science 349, aab3884 (2015).
183. Sawyer, S. et al. Nuclear and mitochondrial DNA sequences from two Denisovan individuals. Proc. Natl Acad. Sci. USA 112, 15696-15700 (2015).
184. Rasmussen, M. et al. The ancestry and affiliations of Kennewick Man. Nature 523, 455-458 (2015).
185. Martiniano, R. et al. Genomic signals of migration and continuity in Britain before the Anglo-Saxons. Nat. Commun. 7, 10326 (2016).
186. Schiffels, S. et al. Iron Age and Anglo-Saxon genomes from East England reveal British migration history. Nat. Commun. 7, 10408 (2016).
187. Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200-205 (2016).
188. Gallego Llorente, M. et al. The genetics of an early Neolithic pastoralist from the Zagros, Iran. Sci. Rep. 6, 31326 (2016).
189. Kilinç, G. M. et al. The demographic development of the first farmers in Anatolia. Curr. Biol. 26, 2659-2666 (2016).
190. Omrak, A. et al. Genomic evidence establishes Anatolia as the source of the European Neolithic gene pool. Curr. Biol. 26, 270-275 (2016).
191. Meyer, M. et al. Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature 531, 504-507 (2016).
192. Skoglund, P. et al. Genomic insights into the peopling of the Southwest Pacific. Nature 538, 510-513 (2016).
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).
194. Unterländer, M. et al. Ancestry and demography and descendants of Iron Age nomads of the Eurasian Steppe. Nat. Commun. 8, 14615 (2017).
195. Lipson, M. et al. Parallel ancient genomic transects reveal complex population history of early European farmers. Preprint at bioRxiv http://dx.doi. org/10.1101/114488 (2017).
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).
197. Kennett, D. J. et al. Archaeogenomic evidence reveals prehistoric matrilineal dynasty. Nat. Commun. 8, 14115 (2017).
198. Mathieson, I. et al. The genomic history of southeastern Europe. Preprint at bioRxiv http://dx. doi.org/10.1101/135616 (2017).
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).
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).
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. http://dx.doi. org/10.1016/j.ajhg.2017.06.013 (2017).
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).
203. Schlebusch, C. M. et al. Ancient genomes from southern Africa pushes modern human divergence beyond 260,000 years ago. Preprint at bioRxiv http://dx.doi.org/10.1101/145409 (2017).
204. Mittnik, A. et al. The genetic history of northern Europe. Preprint at bioRxiv http://dx.doi. org/10.1101/113241 (2017).
205. Slon, V. et al. A fourth Denisovan individual. Sci. Adv. 3, e1700186 (2017).
206. Kuhlwilm, M. et al. Ancient gene flow from early modern humans into Eastern Neanderthals. Nature 530, 429-433 (2016).