by David Reich
Figure 13. This illustration represents the migrations in Europe described in Q. Fu et al., “The Genetic History of Ice Age Europe,” Nature 534 (2016): 200–5. The ice extent is redrawn based on an online figure in “Extent of Ice Sheets in Europe,” Map. Encyclopaedia Britannica Online, https://www.britannica.com/place/Scandinavian-Ice-Sheet?oasmId=54573.
Figure 14. Panel (a) is redrawn based on Extended Data Fig. 4 of W. Haak et al., “Massive Migration from the Steppe Was a Source for Indo-European Languages in Europe,” Nature 522 (2015): 207–11. Panel (b) and its inset are adapted with permission from Fig. 1 and Fig. 2 of D. W. Anthony and D. Ringe, “The Indo-European Homeland from Linguistic and Archaeological Perspectives,” Annual Review of Linguistics 1 (2015): 199–219.
Figure 15. The scatterplots in all three panels are based on the principal component analysis shown in Fig. 1b of I. Lazaridis et al., “Genetic Origins of the Minoans and Mycenaeans,” Nature 548 (2017): 214–8. The x- and y-axes are rotated to roughly align genetic and geographic positions.
Figure 16. The pie charts are based on 180 Bell Beaker individuals for which there is enough ancient DNA data to make relatively precise estimates of steppe-related ancestry. The individuals are grouped by country within present-day Europe. The data are from a revised version of I. Olalde et al., “The Beaker Phenomenon and the Genomic Transformation of Northwest Europe,” bioRxiv (2017): doi.org/10.1101/135962.
Figure 17. In panel (a), the South Asian Language family contours are redrawn based on a plot in A Historical Atlas of South Asia, ed. Joseph E. Schwartzberg (Oxford: Oxford University Press, 1992). In panel (b), the scatterplot is based on the principal component analysis in Fig. 3 of D. Reich et al., “Reconstructing Indian Population History,” Nature 461 (2009): 489–94. The x- and y-axes are rotated to roughly align genetic and geographic positions.
Figure 18. The geographic contours and estimated dates for the spread of wheat and barley agriculture are drawn based on a sketch kindly provided by Dorian Fuller. The contours for the western half of the map follow Fig. 2 of F. Silva and M. Vander Linden, “Amplitude of Travelling Front as Inferred From 14C Predicts Levels of Genetic Admixture Among European Early Farmers,” Scientific Reports 7 (2017): 11985.
Figure 19. The North American ice sheet and shoreline positions are derived from the figures on pages 380–83 of A. S. Dyke, “An Outline of North American Deglaciation with Emphasis on Central and Northern Canada,” Quaternary Glaciations—Extent and Chronology, Part II: North America, ed. Jürgen Ehlers and Philip L. Gibbard (Amsterdam: Elsevier, 2004), 373–422. The Eurasian ice sheet positions are derived from Fig. 4 of H. Patton et al., “Deglaciation of the Eurasian Ice Sheet Complex,” Quaternary Science Reviews 169 (2017): 148–72. The South American ice and shoreline positions are derived form Fig. 5.1 of D. J. Meltzer, “The Origins, Antiquity and Dispersal of the First Americans,” in The Human Past, 4th Edition, ed. Chris Scarre (London: Thames and Hudson, expected early 2018), 149–71. The ancient Siberian shoreline is interpolated.
Figure 20. This illustration combines information from Fig. 2 of D. Reich et al., “Reconstructing Native American Population History,” Nature 488 (2012): 370–74 and Fig. 5 of P. Flegontov et al., “Paleo-Eskimo Genetic Legacy Across North America,” bioRxiv (2017): doi.org/10.1101/203018.
Figure 21. This illustration replots the data from Fig. 1 of P. Skoglund et al., “Genetic Evidence for Two Founding Populations of the Americas,” Nature 525 (2015): 104–8.
Figure 23. The possible migration routes for early speakers of Tai-Kadai, Austroasiatic, and Austronesian languages are drawn based on Fig. 2 of J. Diamond and P. Bellwood, “Farmers and Their Languages: The First Expansions,” Science 300 (2003): 597–603.
Figure 24. The ancient shoreline in panel (1) approximates the map in A. Cooper and C. Stringer, “Did the Denisovans Cross Wallace’s Line?” Science 342 (2013): 321–23.
Figure 25. This illustration is based on Fig. 3D of P. Skoglund et al., “Reconstructing Prehistoric African Population Structure,” Cell 171 (2017): 59–71.
Figure 26. The African language family contours approximate those shown in Fig. 3 of M. C. Campbell, J. B. Hirbo, J. P. Townsend, and S. A. Tishkoff, “The Peopling of the African Continent and the Diaspora into the New World,” Current Opinion in Genetics and Development 29 (2014): 120–32. Possible migratory routes associated with the Bantu expansion are similar to those in Campbell et al., “The Peopling of the African Continent,” but they also incorporate advice from Scott MacEachern and findings from subsequent genetic studies that suggest an expansion north of the tropical rainforest may not have contributed much of the ancestry of present-day Bantu speakers in East Africa (G. B. Busby et al., “Admixture into and Within Sub-Saharan Africa,” eLife 5 (2016): e15266, and E. Patin et al., “Dispersals and Genetic Adaptation of Bantu-Speaking Populations in Africa and North America,” Science 356 (2017): 543–46).
Figure 27. This illustration combines numbers from Fig. 2B and Fig. 2C of P. Skoglund et al., “Reconstructing Prehistoric African Population Structure,” Cell 171 (2017): 59–71.
Figure 28. Adapted with permission from Fig. 2 of M. Karmin et al., “A Recent Bottleneck of Y Chromosome Diversity Coincides with a Global Change in Culture,” Genome Research 25 (2015): 459–66.
Notes
Introduction
1. Luigi Luca Cavalli-Sforza, Paolo Menozzi, and Alberto Piazza, The History and Geography of Human Genes (Princeton, NJ: Princeton University Press, 1994).
2. Luigi Luca Cavalli-Sforza and Francesco Cavalli-Sforza, The Great Human Diasporas: The History of Diversity and Evolution (Reading, MA: Addison-Wesley, 1995).
3. N. A. Rosenberg et al., “Genetic Structure of Human Populations,” Science 298 (2002): 2381–85.
4. P. Menozzi, A. Piazza, and L. L. Cavalli-Sforza, “Synthetic Maps of Human Gene Frequencies in Europeans,” Science 201 (1978): 786–92; L. L. Cavalli-Sforza, P. Menozzi, and A. Piazza, “Demic Expansions and Human Evolution,” Science 259 (1993): 639–46.
5. Albert J. Ammerman and Luigi Luca Cavalli-Sforza, The Neolithic Transition and the Genetics of Populations in Europe (Princeton, NJ: Princeton University Press, 1984).
6. J. Novembre and M. Stephens, “Interpreting Principal Component Analyses of Spatial Population Genetic Variation,” Nature Genetics 40 (2008): 646–49.
7. O. François et al., “Principal Component Analysis Under Population Genetic Models of Range Expansion and Admixture,” Molecular Biology and Evolution 27 (2010): 1257–68.
8. A. Keller et al., “New Insights into the Tyrolean Iceman’s Origin and Phenotype as Inferred by Whole-Genome Sequencing,” Nature Communications 3 (2012): 698; P. Skoglund et al., “Origins and Genetic Legacy of Neolithic Farmers and Hunter-Gatherers in Europe,” Science 336 (2012): 466–69; I. Lazaridis et al., “Ancient Human Genomes Suggest Three Ancestral Populations for Present-Day Europeans,” Nature 513 (2014): 409–13.
9. J. K. Pickrell and D. Reich, “Toward a New History and Geography of Human Genes Informed by Ancient DNA,” Trends in Genetics 30 (2014): 377–89.
10. R. E. Green et al., “A Draft Sequence of the Neandertal Genome,” Science 328 (2010): 710–22.
11. D. Reich et al., “Genetic History of an Archaic Hominin Group from Denisova Cave in Siberia,” Nature 468 (2010): 1053–60.
12. M. Rasmussen et al., “Ancient Human Genome Sequence of an Extinct Palaeo-Eskimo,” Nature 463 (2010): 757–62.
13. W. Haak et al., “Massive Migration from the Steppe Was a Source for Indo-European Languages in Europe,” Nature 522 (2015): 207–11.
14. M. E. Allentoft et al., “Population Genomics of Bronze Age Eurasia,” Nature 522 (2015): 167–72.
15. I. Mathieson et al., “Genome-Wide Patterns of Selection in 230 Ancient Eurasians,” Nature 528 (2015): 499–503.
16. Q. Fu et al., “DNA Analysis of an Early Modern Human from Tianyuan Cave, China,” Proceedings of the National Academy of Sciences of the U.S.A.
110 (2013): 2223–27.
17. H. Shang et al., “An Early Modern Human from Tianyuan Cave, Zhoukoudian, China,” Proceedings of the National Academy of Sciences of the U.S.A. 104 (2007): 6573–78.
18. Haak et al., “Massive Migration.”
19. I. Lazaridis et al., “Genomic Insights into the Origin of Farming in the Ancient Near East,” Nature 536 (2016): 419–24.
20. P. Skoglund et al., “Genomic Insights into the Peopling of the Southwest Pacific,” Nature 538 (2016): 510–13.
21. Lazaridis et al., “Ancient Human Genomes.”
22. Pickrell and Reich, “Toward a New History.”
1 How the Genome Explains Who We Are
1. J. D. Watson and F. H. Crick, “Molecular Structure of Nucleic Acids; a Structure for Deoxyribose Nucleic Acid,” Nature 171 (1953): 737–38.
2. R. L. Cann, M. Stoneking, and A. C. Wilson, “Mitochondrial DNA and Human Evolution,” Nature 325 (1987): 31–36.
3. Cann et al. “Mitochondrial DNA and Human Evolution.”
4. Q. Fu et al., “A Revised Timescale for Human Evolution Based on Ancient Mitochondrial Genomes,” Current Biology 23 (2013): 553–59.
5. D. E. Lieberman, B. M. McBratney, and G. Krovitz, “The Evolution and Development of Cranial Form in Homo sapiens,” Proceedings of the National Academy of Sciences of the U.S.A. 99 (2002):1134–39. Richter et al., “The Age of the Hominin Fossils from Jebel Irhoud, Morocco, and the Origins of the Middle Stone Age,” Nature 546 (2017): 293–96.
6. H. S. Groucutt et al., “Rethinking the Dispersal of Homo sapiens Out of Africa,” Evolutionary Anthropology 24 (2015): 149–64.
7. C.-J. Kind et al., “The Smile of the Lion Man: Recent Excavations in Stadel Cave (Baden-Württemberg, South-Western Germany) and the Restoration of the Famous Upper Palaeolithic Figurine,” Quartär 61 (2014): 129–45.
8. T. Higham et al., “The Timing and Spatiotemporal Patterning of Neanderthal Disappearance,” Nature 512 (2014): 306–9.
9. Richard G. Klein and Blake Edgar, The Dawn of Human Culture (New York: Wiley, 2002).
10. J. Doebley, “Mapping the Genes That Made Maize,” Trends in Genetics 8 (1992): 302–7.
11. S. McBrearty and A. S. Brooks, “The Revolution That Wasn’t: A New Interpretation of the Origin of Modern Human Behavior,” Journal of Human Evolution 39 (2000): 453–563.
12. C. S. L. Lai et al., “A Forkhead-Domain Gene Is Mutated in a Severe Speech and Language Disorder,” Nature 413 (2001): 519–23.
13. W. Enard et al., “Molecular Evolution of FOXP2, a Gene Involved in Speech and Language,” Nature 418 (2002): 869–72.
14. W. Enard et al., “A Humanized Version of FOXP2 Affects Cortico-Basal Ganglia Circuits in Mice,” Cell 137 (2009): 961–71.
15. J. Krause et al., “The Derived FOXP2 Variant of Modern Humans Was Shared with Neandertals,” Current Biology 17 (2007): 1908–12.
16. T. Maricic et al., “A Recent Evolutionary Change Affects a Regulatory Element in the Human FOXP2 Gene,” Molecular Biology and Evolution 30 (2013): 844–52.
17. S. Pääbo, “The Human Condition—a Molecular Approach,” Cell 157 (2014): 216–26.
18. R. E. Green et al., “A Draft Sequence of the Neandertal Genome,” Science 328 (2010): 710–22; K. Prüfer et al., “The Complete Genome Sequence of a Neanderthal from the Altai Mountains,” Nature (2013): doi: 10.1038/nature 1288.
19. R. Lewin, “The Unmasking of Mitochondrial Eve,” Science 238 (1987): 24–26.
20. A. Kong et al., “A High-Resolution Recombination Map of the Human Genome,” Nature Genetics 31 (2002): 241–47.
21. “Descent of Elizabeth II from William I,” Familypedia, http://familypedia.wikia.com/wiki/Descent_of_Elizabeth_II_from_William_I#Shorter_line_of_descent.
22. S. Mallick et al., “The Simons Genome Diversity Project: 300 Genomes from 142 Diverse Populations,” Nature 538 (2016): 201–6.
23. Green et al., “Draft Sequence.”
24. H. Li and R. Durbin, “Inference of Human Population History from Individual Whole-Genome Sequences,” Nature 475 (2011): 493–96.
25. Ibid.
26. S. Schiffels and R. Durbin, “Inferring Human Population Size and Separation History from Multiple Genome Sequences,” Nature Genetics 46 (2014): 919–25.
27. Mallick et al., “Simons Genome Diversity Project.”
28. I. Gronau et al., “Bayesian Inference of Ancient Human Demography from Individual Genome Sequences,” Nature Genetics 43 (2011): 1031–34.
29. Mallick et al., “Simons Genome Diversity Project.”
30. P. C. Sabeti et al., “Detecting Recent Positive Selection in the Human Genome from Haplotype Structure,” Nature 419 (2002): 832–37; B. F. Voight, S. Kudaravalli, X. Wen, and J. K. Pritchard, “A Map of Recent Positive Selection in the Human Genome,” PLoS Biology 4 (2006): e72.
31. K. M. Teshima, G. Coop, and M. Przeworski, “How Reliable Are Empirical Genomic Scans for Selective Sweeps?,” Genome Research 16 (2006): 702–12.
32. R. D. Hernandez et al., “Classic Selective Sweeps Were Rare in Recent Human Evolution,” Science 331 (2011): 920–24.
33. S. A. Tishkoff et al., “Convergent Adaptation of Human Lactase Persistence in Africa and Europe,” Nature Genetics 38 (2006): 31–40.
34. M. C. Turchin et al., “Evidence of Widespread Selection on Standing Variation in Europe at Height-Associated SNPs,” Nature Genetics 44 (2012): 1015–19.
35. I. Mathieson et al., “Genome-Wide Patterns of Selection in 230 Ancient Eurasians,” Nature 528 (2015): 499–503.
36. Y. Field et al., “Detection of Human Adaptation During the Past 2000 Years,” Science 354 (2016): 760–64.
37. D. Welter et al., “The NHGRI GWAS Catalog, a Curated Resource of SNP-Trait Associations,” Nucleic Acids Research 42 (2014): D1001–6.
38. D. B. Goldstein, “Common Genetic Variation and Human Traits,” New England Journal of Medicine 360 (2009): 1696–98.
39. A. Okbay et al., “Genome-Wide Association Study Identifies 74 Loci Associated with Educational Attainment,” Nature 533 (2016): 539–42; M. T. Lo et al., “Genome-Wide Analyses for Personality Traits Identify Six Genomic Loci and Show Correlations with Psychiatric Disorders,” Nature Genetics 49 (2017): 152–56; G. Davies et al., “Genome-Wide Association Study of Cognitive Functions and Educational Attainment in UK Biobank (N=112 151),” Molecular Psychiatry 21 (2016): 758–67.
2 Encounters with Neanderthals
1. Charles Darwin, The Descent of Man, and Selection in Relation to Sex (London: John Murray, 1871).
2. Erik Trinkaus, The Shanidar Neanderthals (New York: Academic Press, 1983).
3. D. Radovčić, A. O. Sršen, J. Radovčić, and D. W. Frayer, “Evidence for Neandertal Jewelry: Modified White-Tailed Eagle Claws at Krapina,” PLoS One 10 (2015): e0119802.
4. J. Jaubert et al., “Early Neanderthal Constructions Deep in Bruniquel Cave in Southwestern France,” Nature 534 (2016): 111–14.
5. W. L. Straus and A. J. E. Cave, “Pathology and the Posture of Neanderthal Man,” Quarterly Review of Biology 32 (1957): 348–63.
6. William Golding, The Inheritors (London: Faber and Faber, 1955).
7. Jean M. Auel, The Clan of the Cave Bear (New York: Crown, 1980).
8. T. Higham et al., “The Timing and Spatiotemporal Patterning of Neanderthal Disappearance,” Nature 512 (2014): 306–9.
9. T. Higham et al., “Chronology of the Grotte du Renne (France) and Implications for the Context of Ornaments and Human Remains Within the Châtelperronian,” Proceedings of the National Academy of Sciences of the U.S.A. 107 (2010): 20234–39; O. Bar-Yosef and J.-G. Bordes, “Who Were the Makers of the Châtelperronian Culture?,” Journal of Human Evolution 59 (2010): 586–93.
10. R. Grün et al., “U-series and ESR Analyses of Bones and Teeth Relating to the Human Burials from Skhul,” Journal of Human Evolution 49 (2005): 316–34.
11. H. Valladas et al., “Thermo-Luminescence Dates for the Neanderthal Burial Site at Ke
bara in Israel,” Nature 330 (1987): 159–60.
12. E. Trinkaus et al., “An Early Modern Human from the Peştera cu Oase, Romania,” Proceedings of the National Academy of Sciences of the U.S.A. 100 (2003): 11231–36.
13. M. Krings et al., “Neandertal DNA Sequences and the Origin of Modern Humans,” Cell 90 (1997): 19–30.
14. C. Posth et al., “Deeply Divergent Archaic Mitochondrial Genome Provides Lower Time Boundary for African Gene Flow into Neanderthals,” Nature Communications 8 (2017): 16046.
15. Krings et al., “Neandertal DNA Sequences.”
16. M. Currat and L. Excoffier, “Modern Humans Did Not Admix with Neanderthals During Their Range Expansion into Europe,” PLoS Biology 2 (2004): e421; D. Serre et al., “No Evidence of Neandertal mtDNA Contribution to Early Modern Humans,” PLoS Biology 2 (2004): e57; M. Nordborg, “On the Probability of Neanderthal Ancestry,” American Journal of Human Genetics 63 (1998): 1237–40.
17. R. E. Green et al., “Analysis of One Million Base Pairs of Neanderthal DNA,” Nature 444 (2006): 330–36.
18. J. D. Wall and S. K. Kim, “Inconsistencies in Neanderthal Genomic DNA Sequences,” PLoS Genetics 3 (2007): 1862–66.
19. Krings et al., “Neandertal DNA Sequences.”
20. S. Sankararaman et al., “The Date of Interbreeding Between Neandertals and Modern Humans,” PLoS Genetics 8 (2012): e1002947.
21. P. Moorjani et al., “A Genetic Method for Dating Ancient Genomes Provides a Direct Estimate of Human Generation Interval in the Last 45,000 Years,” Proceedings of the National Academy of Sciences of the U.S.A. 113 (2016): 5652–7.
22. G. Coop, “Thoughts On: The Date of Interbreeding Between Neandertals and Modern Humans,” Haldane’s Sieve, September 18, 2012, https://haldanessieve.org/2012/09/18/thoughts-on-neandertal-article/.
23. K. Prüfer et al., “The Complete Genome Sequence of a Neanderthal from the Altai Mountains,” Nature (2013): doi: 10.1038/nature 12886.