The expansion of mtDNA haplogroup L3 within and out of Africa

Molecular Biology and Evolution

Volumn 29, Issue 3, 2012, Pages 915-927

  Soares, Pedro ^a   Alshamali, Farida ^b   Pereira, Joana B ^a,c   Fernandes, Verónica ^a,c   Silva, Nuno M ^a   Afonso, Carla ^a   Costa, Marta D ^a,c   Musilová, Eliska ^d   MacAulay, Vincent ^e   Richards, Martin B ^c   Černý, Viktor ^f   Pereira, Luísa ^a,g  

^a UNIVERSITY OF PORTO   (Portugal)

^b Dubai eGovernment Dubai Police   (United Arab Emirates)

^c UNIVERSITY OF LEEDS   (United Kingdom)

^d CHARLES UNIVERSITY   (Czech Republic)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

^f INSTITUTE OF ARCHAEOLOGY   (Czech Republic)

^g University of Porto   (Portugal)

Author keywords

complete genomes; haplogroup L3; modern human expansions; mtDNA; out of Africa

Indexed keywords

MITOCHONDRIAL DNA;

AFRICA; CENTRAL AFRICA; DNA SEQUENCE; HUMAN; HUMAN TISSUE; REVIEW; SEQUENCE ANALYSIS;

AFRICA; AFRICAN CONTINENTAL ANCESTRY GROUP; BASE SEQUENCE; BAYES THEOREM; DNA, MITOCHONDRIAL; EMIGRATION AND IMMIGRATION; EVOLUTION, MOLECULAR; HAPLOTYPES; HISTORY, ANCIENT; HUMANS; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PHYLOGENY; PHYLOGEOGRAPHY; POPULATION DENSITY; POPULATION DYNAMICS; SEQUENCE ANALYSIS, DNA;

EID: 84857059207     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msr245     Document Type: Review

References (87)

1. Ambrose SH. 1998. Chronology of the Later Stone Age and food production in East Africa. J Archaeol Sci. 25:377-392.
2. Andrews RM, Kubacka I, Chinnery PF, Lightowlers R, Turnbull D, Howell N. 1999. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet. 23:147. (Pubitemid 29455385)
3. Armitage SJ, Jasim SA, Marks AE, Parker AG, Usik VI, Uerpmann H-P. 2011. The southern route "Out of Africa": evidence for an early expansion of modern humans into Arabia. Science. 331:453-456.
4. Atkinson QD, Gray RD, Drummond AJ. 2008. mtDNA variation predicts population size in humans and reveals a major Southern Asian chapter in human prehistory. Mol Biol Evol. 25:468-474. (Pubitemid 351231619)
5. Atkinson QD, Gray RD, Drummond AJ. 2009. Bayesian coalescent inference of major human mitochondrial DNA haplogroup expansions in Africa. Philos Trans R Soc Lond B Biol Sci. 276:367-373.
6. Bandelt H-J, Alves-Silva J, Guimarães PEM, et al. (15 co-authors). 2001. Phylogeography of the human mitochondrial haplogroup L3e: a snapshot of African prehistory and the Atlantic slave trade. Ann Hum Genet. 65:549-563. (Pubitemid 34163117)
7. Bandelt H-J, Forster P, Sykes BC, Richards MB. 1995. Mitochondrial portraits of human populations using median networks. Genetics 141:743-753.
8. Bar-Yosef O. 1992. The role of western Asia in modern human origins. Philos Trans R Soc Lond B Biol Sci. 337:193-200. (Pubitemid 23388427)
9. Bar-Yosef O. 1995. The role of climate in the interpretation of human movements and cultural transformations. In: Vrba ES, Denton GH, Partridge TC, Bickele LH, editors. Paleoclimate and evolution, with emphasis on human origins. New Haven (CT): Yale University Press. p. 507-523.
10. Barham L, Mitchell P. 2008. The first Africans: African archaeology from the earliest toolmakers to most recent foragers. Cambridge: Cambridge University Press.
11. Barker G, Barton H, Bird M, et al. (27 co-authors). 2007. The "human revolution" in lowland tropical Southeast Asia: the antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo). J Hum Evol. 52:243-261.
12. Barton RNE, Bouzouggar A, Collcutt SN, Schwenninger J-L, Clark-Balzan L. 2009. OSL dating of the Aterian levels at Dar es-Soltan I (Rabat, Morocco) and implications for the dispersal of modern Homo sapiens. Quat Sci Rev. 28:1914-1931.
13. Basell LS. 2008. Middle Stone Age (MSA) site distributions in eastern Africa and their relationship to Quaternary environmental change, refugia and the evolution of Homo sapiens. Quat Sci Rev. 27:2484-2498.
14. Behar DM, Villems R, Soodyall H, et al. (15 co-authors). 2008. The dawn of human matrilineal diversity. Am J Hum Genet. 82:1130-1140.
15. Beyin A. 2006. The Bab al Mandab vs the Nile-Levant: an appraisal of the two dispersal routes for early modern humans out of Africa. Afr Archaeol Rev. 23:5-30. (Pubitemid 44696348)
16. Bouzouggar A, Barton N, Vanhaeren M, et al. (15 co-authors). 2007. 82,000-year-old shell beads from North Africa and implications for the origins of modern human behavior. Proc Natl Acad Sci USA. 104:9964-9969. (Pubitemid 47175246)
17. Brooks N, Chiapello I, Lernia SD, Drake N, Legrand M, Moulin C, Prospero J. 2005. The climate-environment-society nexus in the Sahara from prehistoric times to the present day. J North Afr Stud. 10:253-292. (Pubitemid 43118266)
18. Bulbeck D. 2007. Where river meets sea: a parsimonious model for Homo sapiens colonization of the Indian Ocean rim and Sahul. Curr Anthropol. 48:315-321.
19. Campbell MC, Tishkoff SA. 2011. The evolution of human genetic and phenotypic variation in Africa. Curr Biol. 20:R166-R173.
20. Cerný V, Fernandes V, Costa MD, Hájek M, Mulligan CJ, Pereira L. 2009. Migration of Chadic speaking pastoralists within Africa based on population structure of Chad Basin and phylogeography of mitochondrial L3f haplogroup. BMC Evol Biol. 9:63.
21. Cerný V, Pereira L, Kujanová M, Vasíková A, Hájek M, Morris M, Mulligan CJ. 2009. Out of Arabia-the settlement of island Soqotra as revealed by mitochondrial and Y chromosome genetic diversity. Am J Phys Anthropol. 138:439-447.
22. Cerný V, Salas A, Hájek M, Zaloudková M, Brdicka R. 2007. A bidirectional corridor in the Sahel-Sudan belt and the distinctive features of the Chad Basin populations: a history revealed by the mitochondrial DNA genome. Ann Hum Genet. 71:433-452. (Pubitemid 46876310)
23. Cherni L, Fernandes V, Pereira JB, et al. (12 co-authors). 2009. Postlast glacial maximum expansion from Iberia to North Africa revealed by fine characterization of mtDNA H haplogroup in Tunisia. Am J Phys Anthropol. 139:253-260.
24. Cohen AS, Stone JR, Beuning KR, et al. (12 co-authors). 2007. Ecological consequences of early Late Pleistocene megadroughts in tropical Africa. Proc Natl Acad Sci USA. 104:16422-16427. (Pubitemid 350211032)
25. Compton JS. 2011. Pleistocene sea-level fluctuations and human evolution on the southerncoastal plain of South Africa. Quat Sci Rev. 30:506-527.
26. d'Errico F, Vanhaeren M, Barton N, Bouzouggar A, Mienis H, Richter D, Hublin J-J, McPherron SP, Lozouet P. 2009. Additional evidence on the use of personal ornaments in the Middle Paleolithic of North Africa. Proc Natl Acad Sci USA. 106:16051-16056.
27. Derricourt R. 2005. Getting "Out of Africa": sea crossings, land crossings and culture in the hominin migrations. J World Prehist. 19:119-132. (Pubitemid 44056343)
28. Drake NA, Blench RM, Armitage SJ, Bristow CS, White KH. 2011. Ancient watercourses and biogeography of the Sahara explain the peopling of the desert. Proc Natl Acad Sci USA. 108:458-462.
29. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:e88.
30. Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 7:214.
31. Drummond AJ, Rambaut A, Shapiro B, Pybus OG. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 22:1185-1192. (Pubitemid 40577756)
32. Endicott P, Ho SYW. 2008. A Bayesian evaluation of human mitochondrial substitution rates. Am J Hum Genet. 82:895-902.
33. Fagundes NJR, Kanitz R, Eckert R, et al. (13 co-authors). 2008. Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am J Hum Genet. 82:583-592.
34. Field JS, Lahr MM. 2005. Assessment of the southern dispersal: GISbased analyses of potential routes at oxygen isotopic stage 4. J World Prehist. 19:1-45. (Pubitemid 43792530)
35. Forster P. 2004. Ice ages and the mitochondrial DNA chronology of human dispersals: a review. Philos Trans R Soc Lond B Biol Sci. 359:255-264. (Pubitemid 38231476)
36. Forster P, Harding R, Torroni A, Bandelt H-J. 1996. Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet. 59:935-945. (Pubitemid 26328092)
37. Gignoux CR, Henn BM, Mountain JL. 2011. Rapid, global demographic expansions after the origins of agriculture. Proc Natl Acad Sci USA. 108:6044-6049.
38. Grün R, Stringer C, McDermott F, Nathan R, Porat N, Robertson S, Taylor L, Mortimer G, Eggins S, McCulloch M. 2005. U-series and ESR analyses of bones and teeth relating to the human burials from Skhul. J Hum Evol. 49:316-334. (Pubitemid 41167416)
39. Harich N, Costa MD, Fernandes V, Kandil M, Pereira JB, Silva NM, Pereira L. 2010. The trans-Saharan slave trade-clues from interpolation analyses and high-resolution characterization of mitochondrial DNA lineages. BMC Evol Biol. 10:138.
40. Haslam M, Clarkson C, Petraglia M, Korisettar R, Bora J, Boivin N, Ditchfield P, Jones S, Mackay A. 2010. Indian lithic technology prior to the 74,000 BP Toba super-eruption: searching for an early modern human signature. In: Boyle V, Gamble C, Bar-Yosef O, editors. Upper palaeolithic revolution in global perspective: essays in honour of Paul Mellars. Cambridge: McDonald Institute for Archaeological Research. p. 73-84.
41. Henshilwood CS, d'Errico F, Watts I. 2009. Engraved ochres from the Middle Stone Age levels at Blombos Cave, South Africa. J Hum Evol. 57:27-47.
42. Henshilwood CS, d'Errico F, Yates R, et al. (11 co-authors). 2002. Emergence of modern human behavior: Middle Stone Age engravings from South Africa. Science 295:1278-1280. (Pubitemid 34157617)
43. Huffman TN. 2007. Handbook to the Iron Age: the archaeology of pre-colonial farming societies in Southern Africa. KwaZulu-Natal (South Africa): University of KwaZulu-Natal Press.
44. Kivisild T, Reidla M, Metspalu E, Rosa A, Brehm A, Pennarun E, Parik J, Geberhiwot T, Usanga E, Villems R. 2004. Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears. Am J Hum Genet. 74:752-770. (Pubitemid 39390485)
45. Kivisild T, Rootsi S, Metspalu M, et al. (18 co-authors). 2003. The genetic heritage of the earliest settlers persists both in Indian tribal and caste populations. Am J Hum Genet. 72:313-332. (Pubitemid 36194241)
46. Klein RG. 1992. The archeology of modern human origins. Evol Anthropol. 1:5-14.
47. Kuper R, Kröpelin S. 2006. Climate-controlled Holocene occupation in the Sahara: motor of Africa's evolution. Science 313:803-807. (Pubitemid 44223342)
48. Lawler A. 2011. Did modern humans travel out of Africa via Arabia? Science 331:387.
49. Macaulay V, Hill C, Achilli A, et al. (21 co-authors). 2005. Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science 308:1034-1036. (Pubitemid 40664416)
50. Mellars P. 2006. Why did modern human populations disperse from Africa ca. 60,000 years ago? A new model. Proc Natl Acad Sci USA. 103:9381-9386. (Pubitemid 43955836)
51. Newman JL. 1995. The peopling of Africa: a geographic interpretation. New Haven (CT): Yale University Press.
52. Olivieri A, Achilli A, Pala M, et al. (15 co-authors). 2006. The mtDNA legacy of the Levantine early Upper Palaeolithic in Africa. Science 314:1767-1770. (Pubitemid 44969086)
53. Oppenheimer S. 2003. Out of Eden. London: Constable and Robinson Ltd.
54. Ottoni C, Primativo G, Hooshiar KB, Achilli A, Martínez-Labarga C, Biondi G, Torroni A, Rickards O. 2010. Mitochondrial haplogroup H1 in North Africa: an early Holocene arrival from Iberia. PLoS One. 5:e13378.
55. Pereira L, Freitas F, Fernandes V, Pereira JB, Costa MD, Costa S, Máximo V, Macaulay V, Rocha R, Samuels DC. 2009. The diversity present in 5140 human mitochondrial genomes. Am J Hum Genet. 84:628-640.
56. Pereira L, Goncalves J, Franco-Duarte R, Silva J, Rocha T, Arnold C, Richards M, Macaulay V. 2007. No evidence for an mtDNA role in sperm motility: data from complete sequencing of asthenozoospermic males. Mol Biol Evol. 24:868-874. (Pubitemid 46355811)
57. Pereira L, Macaulay V, Torroni A, Scozzari R, Prata MJ, Amorim A. 2001. Prehistoric and historic traces in the mtDNA of Mozambique: insights into the Bantu expansions and the slave trade. Ann Hum Genet. 65:439-458. (Pubitemid 33149889)
58. Pereira L, Prata MJ, Amorim A. 2000. Diversity of mtDNA lineages in Portugal: not a genetic edge of European variation. Ann Hum Genet. 64:491-506. (Pubitemid 32166502)
59. Pereira L, Silva NM, Franco-Duarte R, et al. (11 co-authors). 2010. Population expansion in the North African Late Pleistocene signalled by mitochondrial DNA haplogroup U6. BMC Evol Biol. 10:390.
60. Petraglia M, Korisettar R, Boivin N, et al. (14 co-authors). 2007. Middle Paleolithic assemblages from the Indian Subcontinent before and after the Toba super-eruption. Science 317:114-116. (Pubitemid 47056467)
61. Phillipson DW. 2005. African archaeology. Cambridge: Cambridge University Press.
62. Richards M, Bandelt H-J, Kivisild T, Oppenheimer S. 2006. A model for the dispersal of modern humans out of Africa. In: Bandelt H-J, Macaulay V, Richards M, editors. Mitochondrial DNA and the evolution of Homo sapiens. Berlin (Germany): Springer-Verlag. p. 225-265.
63. Richards M, Macaulay V, Hickey E, et al. (37 co-authors). 2000. Tracing European founder lineages in the Near Eastern mtDNA pool. Am J Hum Genet. 67:1251-1276.
64. Richards M, Macaulay V, Hill C, Carracedo A, Salas A. 2004. The archaeogenetics of the Bantu dispersals. In: Jones M, editor. Traces of ancestry: studies in honour of Colin Renfrew. Cambridge: McDonald Institute for Archaeological Research. p. 75-88.
65. Saillard J, Forster P, Lynnerup N, Bandelt H-J, Nørby SS. 2000. mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am J Hum Genet. 67:718-726. (Pubitemid 30659601)
66. Salas A, Richards M, De la Fe T, Lareu M-V, Sobrino B, Sanchez-Diz P, Macaulay V, Carracedo A. 2002. The making of the African mtDNA landscape. Am J Hum Genet. 71:1082-1111. (Pubitemid 35305228)
67. Scheinfeldt LB, Soi S, Tishkoff SA. 2010. Working toward a synthesis of archaeological, linguistic, and genetic data for inferring African population history. Proc Natl Acad Sci USA. 107(Suppl 2):8931-8938.
68. Scholz CA, Johnson TC, Cohen AS, et al. (19 co-authors). 2007. East African megadroughts between 135 and 75 thousands years ago and bearing on early-modern human origins. Proc Natl Acad Sci USA. 104:16416-16421. (Pubitemid 350211031)
69. Shea JJ. 2008. Transitions or turnoversi Climatically-forced extinctions of Homo sapiens and Neanderthals in the east Mediterranean Levant. Quat Sci Rev. 27:2253-2270.
70. Shi W, Ayub Q, Vermeulen M, Shao RG, Zuniga S, van der Gaag K, de Knijff P, Kayser M, Xue Y, Tyler-Smith C. 2010. A worldwide survey of human male demographic history based on Y-SNP and Y-STR data from the HGDP-CEPH populations. Mol Biol Evol. 27:385-393.
71. Soares P, Achilli A, Semino O, Davies W, Macaulay V, Bandelt H-J, Torroni A, Richards MB. 2010. The Archaeogenetics of Europe. Curr Biol. 20:R174-R183.
72. Soares P, Ermini L, Thomson N, Mormina M, Rito T, Röhl A, Salas A, Oppenheimer S, Macaulay V, Richards MB. 2009. Correcting for purifying selection: an improved human mitochondrial molecular clock. Am J Hum Genet. 84:740-759.
73. Soares P, Rito T, Trejaut J, et al. (16 co-authors). 2011. Ancient voyaging and Polynesian origins. Am J Hum Genet. 88:239-247.
74. Soares P, Trejaut JA, Loo J-H, et al. (14 co-authors). 2008. Climate change and postglacial human dispersals in Southeast Asia. Mol Biol Evol. 25:1209-1218.
75. Stager C, Ryves DB, Chase BM, Pausata FSR. 2011. Catastrophic drought in the Afro-Asian monsoon region during Heinrich event 1. Science 331:1299-1302.
76. Texier PJ, Porraz G, Parkington J, et al. (12 co-authors). 2010. A Howiesons Poort tradition of engraving ostrich eggshell containers dated to 60,000 years ago at Diepkloof Rock Shelter, South Africa. Proc Natl Acad Sci USA. 107:6180-6185.
77. Thangaraj K, Chaubey G, Kivisild T, Reddy AG, Singh VK, Rasalkar AA, Singh L. 2005. Reconstructing the origin of Andaman Islanders. Science 308:996. (Pubitemid 40664404)
78. Tishkoff SA, Reed FA, Friedlaender FR, et al. (25 co-authors). 2009. The genetic structure and history of Africans and African Americans. Science 324:1035-1044.
79. Torroni A, Achilli A, Macaulay V, Richards M, Bandelt H-J. 2006. Harvesting the fruit of the human mtDNA tree. Trends Genet. 22:339-345. (Pubitemid 43794927)
80. Turney CSM, Kershaw AP, Moss P, Bird MI, Fifield LK, Cresswell RG, Santos GM, Tada MLD, Hausladen PA, Zhou Y. 2001. Redating the onset of burning at Lynch's Crater (North Queensland): implications for human settlement in Australia. J Quat Sci. 16:767-771. (Pubitemid 34034579)
81. Vanhaeren M, d'Errico F, Stringer C, James SL, Toadd JA, Mienis HK. 2006. Middle Paleolithic shell beads in Israel and Algeria. Science 312:1785-1788. (Pubitemid 43962894)
82. Van Oven M, Kayser M. 2009. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum Mutat. 30:386-394.
83. Watson E, Forster P, Richards M, Bandelt H-J. 1997. Mitochondrial footprints of human expansions in Africa. Am J Hum Genet. 61:691-704. (Pubitemid 27418411)
84. Weldeab S, Lea DW, Schneider RR, Andersen N. 2007. 155,000 years of West African monsoon and ocean thermal evolution. Science 316:1303-1307. (Pubitemid 46871645)
85. Willoughby PR. 2007. The evolution of modern humans in Africa-a comprehensive guide. Lanham (MD): AltaMira Press.
86. Yang Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 13:555-556. (Pubitemid 27480216)
87. Zhivotovsky LA, Underhill PA, Cinnioglu C, et al. (17 co-authors). 2004. The effective mutation rate at Y chromosome short tandem repeats, with application to human populationdivergence time. Am J Hum Genet. 74:50-61. (Pubitemid 38085237)