Evidence for archaic adaptive introgression in humans

Nature Reviews Genetics

Volumn 16, Issue 6, 2015, Pages 359-371

  Racimo, Fernando ^a   Sankararaman, Sriram ^b   Nielsen, Rasmus ^a   Huerta Sánchez, Emilia ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE INTROGRESSION; AFRICAN; ALTITUDE; BALANCING SELECTION; CHROMOSOME 3; DNA SEQUENCE; EUROPEAN; GENE FLOW; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENE SEQUENCE; GENETIC DRIFT; GENETIC SELECTION; GENETIC VARIABILITY; HAPLOTYPE; HIDDEN MARKOV MODEL; HOMO NEANDERTHALENSIS; HOMOZYGOSITY; HUMAN; HUMAN GENETICS; HUMAN GENOME; INTROGRESSION; MELANESIAN; PHYLOGENY; POPULATION STRUCTURE; PRIORITY JOURNAL; REVIEW; STATISTICAL ANALYSIS; ADAPTATION; ANIMAL; BIOLOGICAL MODEL; GENETICS; MOLECULAR EVOLUTION; PROBABILITY;

ADAPTATION, BIOLOGICAL; ANIMALS; EVOLUTION, MOLECULAR; GENE FLOW; GENOME, HUMAN; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; MARKOV CHAINS; MODELS, GENETIC; NEANDERTHALS; PHYLOGENY; SELECTION, GENETIC;

EID: 84929518810     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg3936     Document Type: Review

References (100)

1. Wolpoff, M. H., Wu, X. & Thorne, A. G. in The Origins of Modern Humans: A World Survey of the Fossil Evidence (eds Smith, F. H. & Spencer, F.) 411-483 (Liss, 1984).
2. Stringer, C. B. & Andrews, P. Genetic and fossil evidence for the origin of modern humans. Science 239, 1263-1268 (1988).
3. Bräuer, G. The Afro-European sapiens hypothesis and hominid evolution in East Asia during the late Middle and Upper Pleistocene. Cour. Forschungsinst. Senckenb. 69, 145-165 (1984).
4. Smith, F. H., Janković, I. & Karavanić, I. The assimilation model, modern human origins in Europe, and the extinction of Neandertals. Quaternary Int. 137, 7-19 (2005).
5. Plagnol, V. & Wall, J. D. Possible ancestral structure in human populations. PLoS Genet. 2, e105 (2006).
6. Wall, J. D., Lohmueller, K. E. & Plagnol, V. Detecting ancient admixture and estimating demographic parameters in multiple human populations. Mol. Biol. Evol. 26, 1823-1827 (2009).
7. Higham, T. et al. The timing and spatiotemporal patterning of Neanderthal disappearance. Nature 512, 306-309 (2014).
8. Green, R. E. et al. A draft sequence of the Neandertal genome. Science 328, 710-722 (2010).
9. Prüfer, K. et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505, 43-49 (2014).
10. Reich, D. et al. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468, 1053-1060 (2010).
11. Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222-226 (2012).
12. Castellano, S. et al. Patterns of coding variation in the complete exomes of three Neandertals. Proc. Natl Acad. Sci. USA 111, 6666-6671 (2014).
13. Arnold, M. L. & Martin, N. H. Adaptation by introgression. J. Biol. 8, 82 (2009).
14. Rieseberg, L. H. Evolution: replacing genes and traits through hybridization. Curr. Biol. 19, R119-R122 (2009).
15. Hedrick, P. W. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol. Ecol. 22, 4606-4618 (2013).
16. Hawks, J., Cochran, G., Harpending, H. C. & Lahn, B. T. A genetic legacy from archaic Homo. Trends Genet. 24, 19-23 (2008).
17. Hawks, J. & Cochran, G. Dynamics of adaptive introgression from archaic to modern humans. Paleo Anthropology 2006, 101-115 (2006).
18. Wall, J. D. et al. Higher levels of Neanderthal ancestry in East Asians than in Europeans. Genetics 194, 199-209 (2013).
19. Vernot, B. & Akey, J. M. Resurrecting surviving Neandertal lineages from modern human genomes. Science 343, 1017-1021 (2014).
20. 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).
21. Skoglund, P. & Jakobsson, M. Archaic human ancestry in East Asia. Proc. Natl Acad. Sci. USA 108, 18301-18306 (2011).
22. Hammer, M. F., Woerner, A. E., Mendez, F. L., Watkins, J. C. & Wall, J. D. Genetic evidence for archaic admixture in Africa. Proc. Natl Acad. Sci. USA 108, 15123-15128 (2011).
23. Lachance, J. et al. Evolutionary history and adaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell 150, 457-469 (2012).
24. Veeramah, K. R. & Hammer, M. F. The impact of whole-genome sequencing on the reconstruction of human population history. Nature Rev. Genet. 15, 149-162 (2014).
25. Currat, M. & Excoffier, L. Strong reproductive isolation between humans and Neanderthals inferred from observed patterns of introgression. Proc. Natl Acad. Sci. USA 108, 15129-15134 (2011).
26. Eriksson, A. & Manica, A. Effect of ancient population structure on the degree of polymorphism shared between modern human populations and ancient hominins. Proc. Natl Acad. Sci. USA 109, 13956-13960 (2012).
27. Liang, M. & Nielsen, R. The lengths of admixture tracts. Genetics 197, 953-967 (2014).
28. Pool, J. E. & Nielsen, R. Inference of historical changes in migration rate from the lengths of migrant tracts. Genetics 181, 711-719 (2009).
29. Gravel, S. Population genetics models of local ancestry. Genetics 191, 607-619 (2012).
30. Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from Western Siberia. Nature 514, 445-449 (2014).
31. Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113-1118 (2014).
32. Sankararaman, S., Patterson, N., Li, H., Pääbo, S. & Reich, D. The date of interbreeding between Neandertals and modern humans. PLoS Genet. 8, e1002947 (2012).
33. Gronau, I., Hubisz, M. J., Gulko, B., Danko, C. G. & Siepel, A. Bayesian inference of ancient human demography from individual genome sequences. Nature Genet. 43, 1031-1034 (2011).
34. Gravel, S. et al. Demographic history and rare allele sharing among human populations. Proc. Natl Acad. Sci. USA 108, 11983-11988 (2011).
35. Harris, K. & Nielsen, R. Inferring demographic history from a spectrum of shared haplotype lengths. PLoS Genet. 9, e1003521 (2013).
36. Yang, M. A., Malaspinas, A. S., Durand, E. Y. & Slatkin, M. Ancient structure in Africa unlikely to explain Neanderthal and non-African genetic similarity. Mol. Biol. Evol. 29, 2987-2995 (2012).
37. Lohse, K. & Frantz, L. A. Neandertal admixture in Eurasia confirmed by maximum-likelihood analysis of three genomes. Genetics 196, 1241-1251 (2014).
38. Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065-1093 (2012).
39. Durand, E. Y., Patterson, N., Reich, D. & Slatkin, M. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28, 2239-2252 (2011).
40. Martin, S. H., Davey, J. W. & Jiggins, C. D. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Mol. Biol. Evol. 32, 244-257 (2014).
41. Mendez, F. L., Watkins, J. C. & Hammer, M. F. A haplotype at STAT2 introgressed from Neanderthals and serves as a candidate of positive selection in Papua New Guinea. Am. J. Hum. Genet. 91, 265-274 (2012).
42. Wall, J. D. Detecting ancient admixture in humans using sequence polymorphism data. Genetics 154, 1271-1279 (2000).
43. Viterbi, A. J. Error bounds for convolutional codes and an asymptotically optimum decoding algorithm. IEEE Trans. Inform. Theory 13, 260-269 (1967).
44. Sankararaman, S. et al. The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507, 354-357 (2014).
45. Moorjani, P. et al. The history of African gene flow into Southern Europeans, Levantines, and Jews. PLoS Genet. 7, e1001373 (2011).
46. Voight, B. F., Kudaravalli, S., Wen, X. & Pritchard, J. K. A map of recent positive selection in the human genome. PLoS Biol. 4, e72 (2006).
47. Sabeti, P. C. et al. Detecting recent positive selection in the human genome from haplotype structure. Nature 419, 832-837 (2002).
48. Sabeti, P. C. et al. Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-918 (2007).
49. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 (1989).
50. Fay, J. C. & Wu, C. I. Hitchhiking under positive Darwinian selection. Genetics 155, 1405-1413 (2000).
51. Grossman, S. R. et al. A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327, 883-886 (2010).
52. Barreiro, L. B., Laval, G., Quach, H., Patin, E. & Quintana-Murci, L. Natural selection has driven population differentiation in modern humans. Nature Genet. 40, 340-345 (2008).
53. Lewontin, R. C. & Krakauer, J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74, 175-195 (1973).
54. Shriver, M. D. et al. The genomic distribution of population substructure in four populations using 8,525 autosomal SNPs. Hum. Genom. 1, 274-286 (2004).
55. Yi, X. et al. Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329, 75-78 (2010).
56. Chakraborty, R. Gene admixture in human populations: models and predictions. Am. J. Phys. Anthropol. 29, 1-43 (1986).
57. Huerta-Sánchez, E. et al. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512, 194-197 (2014).
58. Abi-Rached, L. et al. The shaping of modern human immune systems by multiregional admixture with archaic humans. Science 334, 89-94 (2011).
59. Beall, C. M. et al. Natural selection on EPAS1 (HIF2α) associated with low hemoglobin concentration in Tibetan highlanders. Proc. Natl Acad. Sci. USA 107, 11459-11464 (2010).
60. Ding, Q., Hu, Y., Xu, S., Wang, J. & Jin, L. Neanderthal introgression at chromosome 3p21.31 was under positive natural selection in East Asians. Mol. Biol. Evol. 31, 683-695 (2014).
61. Gould, S. J. & Lewontin, R. C. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. 205, 581-598 (1979).
62. Hardy, J. et al. Evidence suggesting that Homo neanderthalensis contributed the H2 MAPT haplotype to Homo sapiens. Biochem. Soc. Trans. 33, 582-585 (2005).
63. Evans, P. D., Mekel-Bobrov, N., Vallender, E. J., Hudson, R. R. & Lahn, B. T. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc. Natl Acad. Sci. USA 103, 18178-18183 (2006).
64. Setó-Salvia, N. et al. Using the neanderthal and denisova genetic data to understand the common MAPT 17q21 inversion in modern humans. Hum. Biol. 84, 633-640 (2012).
65. Ségurel, L., Wyman, M. J. & Przeworski, M. Determinants of mutation rate variation in the human germline. Annu. Rev. Genom. Hum. Genet. 15, 47-70 (2014).
66. Abecasis, G. R. et al. An integrated map of genetic variation from 1,092 human genomes. Nature 491, 56-65 (2012).
67. Khrameeva, E. E. et al. Neanderthal ancestry drives evolution of lipid catabolism in contemporary Europeans. Nature Commun. 5, 3584 (2014).
68. Baselga, J. & Swain, S. M. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nature Rev. Cancer 9, 463-475 (2009).
69. Lalioti, V. et al. The atypical kinase Cdk5 is activated by insulin, regulates the association between GLUT4 and E-Syt1, and modulates glucose transport in 3T3-L1 adipocytes. Proc. Natl Acad. Sci. USA 106, 4249-4253 (2009).
70. 2+-sensor proteins with multiple C2 domains. Proc. Natl Acad. Sci. USA 104, 3823-3828 (2007).
71. DeGiorgio, M., Lohmueller, K. E. & Nielsen, R. A model-based approach for identifying signatures of ancient balancing selection in genetic data. PLoS Genet. 10, e1004561 (2014).
72. Temme, S. et al. A novel family of human leukocyte antigen class II receptors may have its origin in archaic human species. J. Biol. Chem. 289, 639-653 (2014).
73. Ding, Q., Hu, Y. & Jin, L. Non-Neanderthal origin of the HLA-DPB1∗0401. J. Biol. Chem. 289, 10252 (2014).
74. Mendez, F. L., Watkins, J. C. & Hammer, M. F. Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol. Biol. Evol. 30, 798-801 (2013).
75. Mendez, F. L., Watkins, J. C. & Hammer, M. F. Global genetic variation at OAS1 provides evidence of archaic admixture in Melanesian populations. Mol. Biol. Evol. 29, 1513-1520 (2012).
76. Jacobs, L. C. et al. Comprehensive candidate gene study highlights UGT1A and BNC2 as new genes determining continuous skin color variation in Europeans. Hum. Genet. 132, 147-158 (2013).
77. Eriksson, N. et al. Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet. 6, e1000993 (2010).
78. Ding, Q. et al. Neanderthal origin of the haplotypes carrying the functional variant Val92Met in the MC1R in modern humans. Mol. Biol. Evol. 31, 1994-2003 (2014).
79. Nachman, M. W., Hoekstra, H. E. & D'Agostino, S. L. The genetic basis of adaptive melanism in pocket mice. Proc. Natl Acad. Sci. USA 100, 5268-5273 (2003).
80. Valverde, P. et al. The Asp84Glu variant of the melanocortin 1 receptor (MC1R) is associated with melanoma. Hum. Mol. Genet. 5, 1663-1666 (1996).
81. Valverde, P., Healy, E., Jackson, I., Rees, J. L. & Thody, A. J. Variants of the melanocyte-stimulating hormone receptor gene are associated with red hair and fair skin in humans. Nature Genet. 11, 328-330 (1995).
82. Fu, Y. X. & Li, W. H. Statistical tests of neutrality of mutations. Genetics 133, 693-709 (1993).
83. Altshuler, D. M. et al. Integrating common and rare genetic variation in diverse human populations. Nature 467, 52-58 (2010).
84. Bigham, A. et al. Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet. 6, e1001116 (2010).
85. Simonson, T. S. et al. Genetic evidence for high-altitude adaptation in Tibet. Science 329, 72-75 (2010).
86. Peng, Y. et al. Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol. Biol. Evol. 28, 1075-1081 (2011).
87. Xu, S. et al. A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol. Biol. Evol. 28, 1003-1011 (2011).
88. Wang, B. et al. On the origin of Tibetans and their genetic basis in adapting high-altitude environments. PLoS ONE 6, e17002 (2011).
89. Abecasis, G. R. et al. A map of human genome variation from population-scale sequencing. Nature 467, 1061-1073 (2010).
90. Williams, A. L. et al. Sequence variants in SLC16A11 are a common risk factor for type 2 diabetes in Mexico. Nature 506, 97-101 (2014).
91. Zietkiewicz, E. et al. Haplotypes in the dystrophin DNA segment point to a mosaic origin of modern human diversity. Am. J. Hum. Genet. 73, 994-1015 (2003).
92. Yotova, V. et al. An X-linked haplotype of Neandertal origin is present among all non-African populations. Mol. Biol. Evol. 28, 1957-1962 (2011).
93. Moorjani, P. et al. Genetic evidence for recent population mixture in India. Am. J. Hum. Genet. 93, 422-438 (2013).
94. Hellenthal, G. et al. A genetic atlas of human admixture history. Science 343, 747-751 (2014).
95. Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409-413 (2014).
96. Huerta-Sánchez, E. et al. Genetic signatures reveal high-altitude adaptation in a set of Ethiopian populations. Mol. Biol. Evol. 30, 1877-1888 (2013).
97. Jeong, C. et al. Admixture facilitates genetic adaptations to high altitude in Tibet. Nature Commun. 5, 3281 (2014).
98. Bhatia, G. et al. Genome-wide scan of 29,141 African Americans finds no evidence of directional selection since admixture. Am. J. Hum. Genet. 95, 437-444 (2014).
99. Waddell, P. J. Happy New Year Homo erectus? More evidence for interbreeding with archaics predating the modern human/Neanderthal split. arXiv [online], http://arxiv.org/abs/1312.7749 (2013).
100. Waddell, P. J. & Tan, X. New g%AIC, g%AICc, g%BIC, and power divergence fit statistics expose mating between modern humans, Neanderthals and other archaics. arXiv [online], http://arxiv.org/abs/1212.6820 (2012).