Model-based analyses of whole-genome data reveal a complex evolutionary history involving archaic introgression in Central African Pygmies

Genome Research

Volumn 26, Issue 3, 2016, Pages 291-300

  Hsieh, PingHsun ^a   Woerner, August E ^b,c   Wall, Jeffrey D ^d   Lachance, Joseph ^e,f   Tishkoff, Sarah A ^e   Gutenkunst, Ryan N ^a   Hammer, Michael F ^c  

^a University of Arizona   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ARTICLE; CENTRAL AFRICAN; DEMOGRAPHY; EVOLUTION; GENE FLOW; GENOME; HISTORY; HOMINID; HUMAN; INTROGRESSION; ISOLATION PROCEDURE; PRIORITY JOURNAL; PYGMY; SIMULATION; ANIMAL; BLACK PERSON; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETICS; GENOMICS; HAPLOTYPE; HUMAN GENOME; MOLECULAR EVOLUTION; PAN PANISCUS; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

AFRICAN CONTINENTAL ANCESTRY GROUP; ANIMALS; EVOLUTION, MOLECULAR; GENE FLOW; GENE FREQUENCY; GENETIC LOCI; GENETICS, POPULATION; GENOME; GENOME, HUMAN; GENOMICS; HAPLOTYPES; HUMANS; LINKAGE DISEQUILIBRIUM; PAN PANISCUS; POLYMORPHISM, SINGLE NUCLEOTIDE;

EID: 84960458307     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.196634.115     Document Type: Article

References (73)

1. Bandelt HJ, Forster P, Rohl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37-48.
2. Bräuer G. 2008. The origin of modern anatomy: by speciation or intraspecific evolution? Evol Anthropol 17:22-37.
3. Browning SR, Browning BL. 2007. Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81:1084-1097.
4. Campana MG, Bower MA, Crabtree PJ. 2013. Ancient DNA for the archaeologist: the future of African research. Afr Archaeol Rev 30:21-37.
5. Cavalli-Sforza LL, Menozzi P, Piazza A. 1994. The history and geography of human genes. Princeton University Press, Princeton, NJ.
6. Chen GK, Marjoram P, Wall JD. 2009. Fast and flexible simulation of DNA sequence data. Genome Res 19:136-142.
7. De Menocal PB. 2011. Anthropology. Climate and human evolution. Science 331:540-542.
8. Drmanac R, Sparks AB, Callow MJ, Halpern AL, Burns NL, Kermani BG, Carnevali P, Nazarenko I, Nilsen GB, Yeung G, et al. 2010. Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science 327:78-81.
9. Evans PD, Mekel-Bobrov N, Vallender EJ, Hudson RR, Lahn BT. 2006. Evidence that the adaptive allele of the brain size gene microcephalin introgressed into Homo sapiens from an archaic Homo lineage. Proc Natl Acad Sci 103:18178-18183.
10. Fenner JN. 2005. Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am J Phys Anthropol 128:415-423.
11. Fu Q, Li H, Moorjani P, Jay F, Slepchenko SM, Bondarev AA, Johnson PL, Aximu-Petri A, Prüfer K, De Filippo C, et al. 2014. Genome sequence of a 45, 000-year-old modern human from western Siberia. Nature 514:445-449.
12. Gallego Llorente M, Jones ER, Eriksson A, Siska V, Arthur KW, Arthur JW, Curtis MC, Stock JT, Coltorti M, Pieruccini P, et al. 2015. Ancient Ethiopian genome reveals extensive Eurasian admixture throughout the African continent. Science 350:820-822.
13. Garrigan D, Mobasher Z, Kingan SB, Wilder JA, Hammer MF. 2005. Deep haplotype divergence and long-range linkage disequilibrium at Xp21.1 provide evidence that humans descend from a structured ancestral population. Genetics 170:1849-1856.
14. Glazko GV, Nei M. 2003. Estimation of divergence times for major lineages of primate species. Mol Biol Evol 20:424-434.
15. Gravel S. 2012. Population genetics models of local ancestry. Genetics 191:607-619.
16. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MH, et al. 2010. A draft sequence of the Neandertal genome. Science 328:710-722.
17. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. 2009. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5:e1000695.
18. Hammer MF. 2013. Human hybrids. Sci Am 308:66-71.
19. Hammer MF, Woerner AE, Mendez FL, Watkins JC, Wall JD. 2011. Genetic evidence for archaic admixture in Africa. Proc Natl Acad Sci 108:15123-15128.
20. Hardy J, Pittman A, Myers A, Gwinn-Hardy K, Fung HC, De Silva R, Hutton M, Duckworth J. 2005. Evidence suggesting that Homo neanderthalensis contributed the H2 MAPT haplotype to Homo sapiens. Biochem Soc Transac 33(Pt 4):582-585.
21. Hartl DL, Clark AG, Clark AG. 1997. Principles of population genetics. Sinauer Associates, Sunderland, MA.
22. Harvati K, Stringer C, Grün R, Aubert M, Allsworth-Jones P, Folorunso CA. 2011. The Later Stone Age calvaria from Iwo Eleru, Nigeria: morphology and chronology. PLoS One 6:e24024.
23. Hayakawa T, Aki I, Varki A, Satta Y, Takahata N. 2006. Fixation of the human-specific CMP-N-acetylneuraminic acid hydroxylase pseudogene and implications of haplotype diversity for human evolution. Genetics 172:1139-1146.
24. Hinch AG, Tandon A, Patterson N, Song Y, Rohland N, Palmer CD, Chen GK, Wang K, Buxbaum SG, Akylbekova EL, et al. 2011. The landscape of recombination in African Americans. Nature 476:170-175.
25. Hsieh P, Veeramah KR, Lachance J, Tishkoff SA, Wall JD, Hammer MF, Gutenkunst RN. 2016. Whole-genome sequence analyses of Western Central African Pygmy hunter-gatherers reveal a complex demographic history and identify candidate genes under positive natural selection. Genome Res (this issue) 26:279-290.
26. Huerta-Sánchez E, Jin X, Asan, Bianba Z, Peter BM, Vinckenbosch N, Liang Y, Yi X, He M, Somel M, et al. 2014. Altitude adaptation in Tibetans caused by introgression of Denisovan-like DNA. Nature 512:194-197.
27. The International HapMap Consortium. 2007. A second generation human haplotype map of over 3.1 million SNPs. Nature 449:851-861.
28. Jarvis JP, Scheinfeldt LB, Soi S, Lambert C, Omberg L, Ferwerda B, Froment A, Bodo JM, Beggs W, Hoffman G, et al. 2012. Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African Pygmies. PLoS Genet 8:e1002641.
29. Kim BY, Lohmueller KE. 2015. Selection and reduced population size cannot explain higher amounts of Neandertal ancestry in East Asian than in European human populations. Am J Hum Genet 96:454-461.
30. Lachance J, Vernot B, Elbers CC, Ferwerda B, Froment A, Bodo JM, Lema G, Fu W, Nyambo TB, Rebbeck TR, et al. 2012. Evolutionary history and adaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell 150:457-469.
31. Langergraber KE, Prüfer K, Rowney C, Boesch C, Crockford C, Fawcett K, Inoue E, Inoue-Muruyama M, Mitani JC, Muller MN, et al. 2012. Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci 109:15716-15721.
32. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, Cann HM, Barsh GS, Feldman M, Cavalli-Sforza LL, et al. 2008. Worldwide human relationships inferred from genome-wide patterns of variation. Science 319:1100-1104.
33. Li S, Schlebusch C, Jakobsson M. 2014. Genetic variation reveals large-scale population expansion and migration during the expansion of Bantuspeaking peoples. Proc Biol Sci 281:20141448.
34. Liang M, Nielsen R. 2014. The lengths of admixture tracts. Genetics 197:953-967.
35. Loh PR, Lipson M, Patterson N, Moorjani P, Pickrell JK, Reich D, Berger B. 2013. Inferring admixture historiesof human populations using linkage disequilibrium. Genetics 193:1233-1254.
36. Mallet J. 2007. Hybrid speciation. Nature 446:279-283.
37. Mendez FL, Watkins JC, Hammer MF. 2012. A haplotype at STAT2 introgressed from Neanderthals and servesasacandidate ofpositive selection in Papua New Guinea. Am J Hum Genet 91:265-274.
38. Mendez FL, Watkins JC, Hammer MF. 2013. Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol Biol Evol 30:798-801.
39. Moorjani P, Patterson N, Hirschhorn JN, Keinan A, Hao L, Atzmon G, Burns E, Ostrer H, Price AL, Reich D. 2011. The history of African gene flow into Southern Europeans, Levantines, and Jews. PLoS Genet 7:e1001373.
40. Moorjani P, Thangaraj K, Patterson N, Lipson M, Loh PR, Govindaraj P, Berger B, Reich D, Singh L. 2013. Genetic evidencefor recent population mixture in India. Am J Hum Genet 93:422-438.
41. Ohta T, Kimura M. 1969. Linkage disequilibrium at steady state determined by random genetic drift and recurrent mutation. Genetics 63:229-238.
42. Pääbo S. 2014. The human condition-a molecular approach. Cell 157:216-226.
43. Patin E, Laval G, Barreiro LB, Salas A, Semino O, Santachiara-Benerecetti S, Kidd KK, Kidd JR, Van Der Veen L, Hombert JM, et al. 2009. Inferring the demographic history of African farmers and Pygmy hunter-gatherers using a multilocus resequencing data set. PLoS Genet 5:e1000448.
44. Phillipson DW. 2005. African archaeology. Cambridge University Press, New York.
45. Pickrell JK, Patterson N, Barbieri C, Berthold F, Gerlach L, Guldemann T, Kure B, Mpoloka SW, Nakagawa H, Naumann C, et al. 2012. The genetic prehistory of southern Africa. Nat Commun 3:1143.
46. Pickrell JK, Patterson N, Loh PR, Lipson M, Berger B, Stoneking M, Pakendorf B, Reich D. 2014. Ancient west Eurasian ancestry in southern and eastern Africa. Proc Natl Acad Sci 111:2632-2637.
47. Plagnol V, Wall JD. 2006. Possible ancestral structure in human populations. PLoS Genet 2:e105.
48. Pool JE, Nielsen R. 2009. Inference of historical changes in migration rate from the lengths of migrant tracts. Genetics 181:711-719.
49. Potts R. 2013. Hominin evolution in settings of strong environmental variability. Quat Sci Rev 73:1-13.
50. Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, De Filippo C, et al. 2014. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43-49.
51. R Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
52. Racimo F, Sankararaman S, Nielsen R, Huerta-Sánchez E. 2015. Evidence for archaic adaptive introgression in humans. Nat Rev Genet 16:359-371.
53. Reich D, Green RE, Kircher M, Krause J, Patterson N, Durand EY, Viola B, Briggs AW, Stenzel U, Johnson PL, et al. 2010. Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053-1060.
54. Reich D, Patterson N, Kircher M, Delfin F, Nandineni MR, Pugach I, Ko AM, Ko YC, Jinam TA, Phipps ME, et al. 2011. Denisova admixture and the first modern human dispersals into Southeast Asia and Oceania. Am J Hum Genet 89:516-528.
55. Rightmire GP. 2009. Out of Africa: modern human origins special feature: middle and later Pleistocene hominins in Africa and Southwest Asia. Proc Natl Acad Sci 106:16046-16050.
56. Rogers AR, Huff C. 2009. Linkage disequilibrium between loci with unknown phase. Genetics 182:839-844.
57. Sankararaman S, Patterson N, Li H, Pääbo S, Reich D. 2012. The date of interbreeding between Neandertals and modern humans. PLoS Genet 8:e1002947.
58. Sankararaman S, Mallick S, Dannemann M, Prüfer K, Kelso J, Pääbo S, Patterson N, Reich D. 2014. The genomic landscape of Neanderthal ancestry in present-day humans. Nature 507:354-357.
59. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci 100:9440-9445.
60. Stringer C. 2012. Lone survivors: how we came to be the only humans on earth. Macmillan, New York.
61. Thomson R, Pritchard JK, Shen P, Oefner PJ, Feldman MW. 2000. Recent common ancestry of human Y chromosomes: evidence from DNA sequence data. Proc Natl Acad Sci 97:7360-7365.
62. Tishkoff SA, Reed FA, Friedlaender FR, Ehret C, Ranciaro A, Froment A, Hirbo JB, Awomoyi AA, Bodo JM, Doumbo O, et al. 2009. The genetic structure and history of Africans and African Americans. Science 324:1035-1044.
63. Twyford AD, Ennos RA. 2012. Next-generation hybridization and introgression. Heredity 108:179-189.
64. Veeramah KR, Hammer MF. 2014. The impactof whole-genome sequencing on the reconstruction of human population history. Nat Rev Genet 15:149-162.
65. Vernot B, Akey JM. 2014. Resurrecting surviving Neandertal lineages from modern human genomes. Science 343:1017-1021.
66. Vernot B, Akey JM. 2015. Complex history of admixture between modern humans and Neandertals. Am J Hum Genet 96:448-453.
67. Villmoare B, Kimbel WH, Seyoum C, Campisano CJ, Di Maggio EN, Rowan J, Braun DR, Arrowsmith JR, Reed KE. 2015. Paleoanthropology. Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia. Science 347:1352-1355.
68. Wall JD. 2000. Detecting ancient admixture in humans using sequence polymorphism data. Genetics 154:1271-1279.
69. Wall JD, Hammer MF. 2006. Archaic admixture in the human genome. Curr Opin Genet Dev 16:606-610.
70. Wall JD, Lohmueller KE, Plagnol V. 2009. Detecting ancient admixture and estimating demographic parameters in multiple human populations. Mol Biol Evol 26:1823-1827.
71. Wang S, Lachance J, Tishkoff SA, Hey J, Xing J. 2013. Apparent variation in Neanderthal admixture among African populations is consistent with gene flow from non-African populations. Genome Biol Evol 5:2075-2081.
72. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R. 2007. Localizing recent adaptive evolution in the human genome. PLoS Genet 3:e90.
73. Zinner D, Arnold ML, Roos C. 2011. The strange blood: natural hybridization in primates. Evol Anthropol 20:96-103.