Following the Evolution of Homo Sapiens across Africa using a Uniparental Genetic Guide

Main Article Content

Vicente Martinez Cabrera

Abstract

The origin and evolution of modern humans in Africa has reached a multidisciplinary consensus but the age and regions where it originated and evolved are current topics of discussion. In this study I put forward an integrative model guided by the phylogeny and phylogeography of mitochondrial DNA and Y-chromosome haplogroups. I propose an early origin of modern humans in northwest Africa in a temporal window of 257-345 thousand years ago. A first population split in central Africa around 175-288 thousand years ago. A subsequent northward spread with additional population subdivisions during a long statistical interval that culminated in a first successful out of Africa migration around 130 thousand years ago. A population constriction in southwest Asia motivated an early return to Africa between 70 and 100 thousand years ago. This ample Eurasian-ebb to Africa, detected by mitochondrial haplogroup L3 and Y-chromosome haplogroup E preceded other later and geographically more limited Eurasian backflows. The archaeological and fossil finds that could be coetaneous to this molecular journey have been integrated into this interdisciplinary model.

Article Details

How to Cite
CABRERA, Vicente Martinez. Following the Evolution of Homo Sapiens across Africa using a Uniparental Genetic Guide. Medical Research Archives, [S.l.], v. 11, n. 1, jan. 2023. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/3460>. Date accessed: 29 mar. 2024. doi: https://doi.org/10.18103/mra.v11i1.3460.
Section
Research Articles

References

1. Lewin R. Human evolution: an illustrated introduction. John Wiley \& Sons; 2009.

2. Cann RL, Stoneking M, Wilson AC. Mitochondrial DNA and human evolution. Nature. 1987;325(6099):31-36.

3. Watson E, Forster P, Richards M, Bandelt H-J. Mitochondrial footprints of human expansions in Africa. The American Journal of Human Genetics. 1997;61(3):691-704.

4. Richter D, Grün R, Joannes-Boyau R, et al. The age of the hominin fossils from Jebel Irhoud, Morocco, and the origins of the Middle Stone Age. Nature. 2017;546(7657):293-296.

5. Hublin J-J, Ben-Ncer A, Bailey SE, et al. New fossils from Jebel Irhoud, Morocco and the pan-African origin of Homo sapiens. Nature. 2017;546(7657):289-292.

6. Brooks AS, Yellen JE, Potts R, et al. Long-distance stone transport and pigment use in the earliest Middle Stone Age. Science. 2018;360(6384):90-94.

7. Deino AL, Behrensmeyer AK, Brooks AS, Yellen JE, Sharp WD, Potts R. Chronology of the Acheulean to Middle Stone Age transition in eastern Africa. Science. 2018;360(6384):95-98.

8. Hershkovitz I, Weber GW, Quam R, et al. The earliest modern humans outside Africa. Science. 2018;359(6374):456-459.

9. Liu W, Martinón-Torres M, Cai Y, et al. The earliest unequivocally modern humans in southern China. Nature. 2015;526(7575):696-699.

10. Pagani L, Lawson DJ, Jagoda E, et al. Genomic analyses inform on migration events during the peopling of Eurasia. Nature. 2016;538(7624):238-242.

11. Malaspinas A-S, Westaway MC, Muller C, et al. A genomic history of Aboriginal Australia. Nature. 2016;538(7624):207-214.

12. Mallick S, Li H, Lipson M, et al. The Simons genome diversity project: 300 genomes from 142 diverse populations. Nature. 2016;538(7624):201-206.

13. Bergstrӧm A, Stringer C, Hajdinjak M, Scerri EM, Skoglund P. Origins of modern human ancestry. Nature. 2021;590(7845):229-237.

14. Cabrera VM. Human molecular evolutionary rate, time dependency and transient polymorphism effects viewed through ancient and modern mitochondrial DNA genomes. Scientific Reports. 2021;11(1):1-8.

15. Scally A, Durbin R. Revising the human mutation rate: implications for understanding human evolution. Nat Rev Genet. 2012;13(10):745-53. doi:10.1038/nrg3295.

16. Zaidi AA, Wilton PR, Su MS-W, et al. Bottleneck and selection in the germline and maternal age influence transmission of mitochondrial DNA in human pedigrees. Proceedings of the National Academy of Sciences. 2019;116(50):25172-25178.

17. Rebolledo-Jaramillo B, Su MS-W, Stoler N, et al. Maternal age effect and severe germ-line bottleneck in the inheritance of human mitochondrial DNA. Proceedings of the National Academy of Sciences. 2014;111(43):15474-15479.

18. Soares P, Ermini L, Thomson N, et al. Correcting for purifying selection: an improved human mitochondrial molecular clock. The American Journal of Human Genetics. 2009;84(6):740-759.

19. Henn BM, Gignoux CR, Feldman MW, Mountain JL. Characterizing the time dependency of human mitochondrial DNA mutation rate estimates. Molecular biology and evolution. 2009;26(1):217-230.

20. Ho SYW, Larson G. Molecular clocks: when times are a-changin’. Trends Genet. 2006;22(2):79-83.

21. Cabrera VM. Counterbalancing the time-dependent effect on the human mitochondrial DNA molecular clock. BMC Evolutionary Biology. 2020;20(1):1-9.

22. Van Oven M, Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Human mutation. 2009;30(2):E386-E394.

23. Cabrera VM, Marrero P, Abu-Amero KK, Larruga JM. Carriers of mitochondrial DNA macrohaplogroup L3 basal lineages migrated back to Africa from Asia around 70,000 years ago. BMC evolutionary biology. 2018;18(1):1-16.

24. Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999;16(1):37-48.

25. Forster P, Harding R, Torroni A, Bandelt HJ. Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet. 1996;59(4):935-45.

26. Schwartz JH, Tattersall I. Defining the genus Homo. Science. 2015;349(6251):931-932.

27. Barash A, Belmaker M, Bastir M, et al. The earliest Pleistocene record of a large-bodied hominin from the Levant supports two out-of-Africa dispersal events. Scientific reports. 2022;12(1):1-9.

28. Herries AI, Martin JM, Leece A, et al. Contemporaneity of Australopithecus, Paranthropus, and early Homo erectus in South Africa. Science. 2020;368(6486):eaaw7293.

29. Belmaker M, Tchernov E, Condemi S, Bar-Yosef O. New evidence for hominid presence in the Lower Pleistocene of the Southern Levant. Journal of Human Evolution. 2002;43(1):43-56.

30. Lordkipanidze D, Ponce de León MS, Margvelashvili A, et al. A complete skull from Dmanisi, Georgia, and the evolutionary biology of early Homo. Science. 2013;342(6156):326-331.

31. Zhu Z-Y, Dennell R, Huang W-W, et al. New dating of the Homo erectus cranium from Lantian (Gongwangling), China. Journal of Human Evolution. 2015;78:144-157.

32. Matsu’ura S, Kondo M, Danhara T, et al. Age control of the first appearance datum for Javanese Homo erectus in the Sangiran area. Science. 2020;367(6474):210-214.

33. Rightmire GP. Homo erectus and Middle Pleistocene hominins: brain size, skull form, and species recognition. Journal of Human Evolution. 2013;65(3):223-252.

34. Hedges SB, Marin J, Suleski M, Paymer M, Kumar S. Tree of life reveals clock-like speciation and diversification. Molecular biology and evolution. 2015;32(4):835-845.

35. Green RE, Malaspinas A-S, Krause J, et al. A complete Neandertal mitochondrial genome sequence determined by high-throughput sequencing. Cell. 2008;134(3):416-426.

36. Meyer M, Fu Q, Aximu-Petri A, et al. A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature. 2014;505(7483):403-406.

37. Meyer M, Arsuaga J-L, de Filippo C, et al. Nuclear DNA sequences from the Middle Pleistocene Sima de los Huesos hominins. Nature. 2016;531(7595):504-507.

38. Slon V, Mafessoni F, Vernot B, et al. The genome of the offspring of a Neanderthal mother and a Denisovan father. Nature. 2018;561(7721):113-116.

39. Smith FH, Ahern JC, Jankovi’c I, Karavani’c I. The Assimilation Model of modern human origins in light of current genetic and genomic knowledge. Quaternary International. 2017;450:126-136.

40. Shea JJ. Neandertals, competition, and the origin of modern human behavior in the Levant. Evolutionary Anthropology: Issues, News, and Reviews: Issues, News, and Reviews. 2003;12(4):173-187.

41. Etler DA. Homo erectusin East Asia: Human Ancestor or Evolutionary Dead-End? gene. 1984;1992:2001.

42. Slimak L, Zanolli C, Higham T, et al. Modern human incursion into Neanderthal territories 54,000 years ago at Mandrin, France. Science Advances. 2022;8(6):eabj9496.

43. Vaesen K, Dusseldorp GL, Brandt MJ. An emerging consensus in palaeoanthropology: demography was the main factor responsible for the disappearance of Neanderthals. Scientific reports. 2021;11(1):1-9.

44. Dalén L, Orlando L, Shapiro B, et al. Partial genetic turnover in neandertals: continuity in the east and population replacement in the west. Molecular biology and evolution. 2012;29(8):1893-1897.

45. Hublin J-J, Sirakov N, Aldeias V, et al. Initial upper palaeolithic homo sapiens from bacho kiro cave, Bulgaria. Nature. 2020;581(7808):299-302.

46. Prüfer K, Posth C, Yu H, et al. A genome sequence from a modern human skull over 45,000 years old from Zlat\`y k\uu\vn in Czechia. Nature ecology \& evolution. 2021;5(6):820-825.

47. Mendez FL, Poznik GD, Castellano S, Bustamante CD. The divergence of Neandertal and modern human Y chromosomes. The American Journal of Human Genetics. 2016;98(4):728-734.

48. Meyer M, Kircher M, Gansauge M-T, et al. A high-coverage genome sequence from an archaic Denisovan individual. Science. 2012;338(6104):222-226.

49. Petr M, Hajdinjak M, Fu Q, et al. The evolutionary history of Neanderthal and Denisovan Y chromosomes. Science. 2020;369(6511):1653-1656.

50. Cabrera VM. Journal of Phylogenetics & Evolutionary Biology. 2021;9(8):171.

51. Prüfer K, Racimo F, Patterson N, et al. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature. 2014;505(7481):43-49.

52. Van de Loosdrecht M, Bouzouggar A, Humphrey L, et al. Pleistocene North African genomes link near Eastern and sub-Saharan African human populations. Science. 2018;360(6388):548-552.

53. Fregel R, Méndez FL, Bokbot Y, et al. Ancient genomes from North Africa evidence prehistoric migrations to the Maghreb from both the Levant and Europe. Proceedings of the National Academy of Sciences. 2018;115(26):6774-6779.

54. Arredi B, Poloni ES, Paracchini S, et al. A predominantly neolithic origin for Y-chromosomal DNA variation in North Africa. The American Journal of Human Genetics. 2004;75(2):338-345.

55. Cruciani F, Trombetta B, Massaia A, Destro-Bisol G, Sellitto D, Scozzari R. A revised root for the human Y chromosomal phylogenetic tree: the origin of patrilineal diversity in Africa. The American Journal of Human Genetics. 2011;88(6):814-818.

56. Grün R, Pike A, McDermott F, et al. Dating the skull from Broken Hill, Zambia, and its position in human evolution. Nature. 2020;580(7803):372-375.

57. Bräuer G, Yokoyama Y, Falguères C, Mbua E, others. Modern human origins backdated. Nature. 1997;386(6623):337-338.

58. Fan S, Kelly DE, Beltrame MH, et al. African evolutionary history inferred from whole genome sequence data of 44 indigenous African populations. Genome Biology. 2019;20(1):1-14.

59. Chan EK, Hardie R-A, Petersen DC, et al. Revised timeline and distribution of the earliest diverged human maternal lineages in southern Africa. PloS one. 2015;10(3):e0121223.

60. Batini C, Lopes J, Behar DM, et al. Insights into the demographic history of African Pygmies from complete mitochondrial genomes. Molecular biology and evolution. 2011;28(2):1099-1110.

61. Barbieri C, Hübner A, Macholdt E, et al. Refining the Y chromosome phylogeny with southern African sequences. Human genetics. 2016;135(5):541-553.

62. Naidoo T, Xu J, Vicente M, et al. Y-chromosome variation in Southern African Khoe-San populations based on whole-genome sequences. Genome biology and evolution. 2020;12(7):1031-1039.

63. Martiniano R, De Sanctis B, Hallast P, Durbin R. Placing ancient DNA sequences into reference phylogenies. Molecular biology and evolution. 2022;39(2):msac017.

64. Scozzari R, Massaia A, Trombetta B, et al. An unbiased resource of novel SNP markers provides a new chronology for the human Y chromosome and reveals a deep phylogenetic structure in Africa. Genome research. 2014;24(3):535-544.

65. Batini C, Ferri G, Destro-Bisol G, et al. Signatures of the preagricultural peopling processes in sub-Saharan Africa as revealed by the phylogeography of early Y chromosome lineages. Molecular biology and evolution. 2011;28(9):2603-2613.

66. Schlebusch CM, Malmstrӧm H, Günther T, et al. Southern African ancient genomes estimate modern human divergence to 350,000 to 260,000 years ago. Science. 2017;358(6363):652-655.

67. Schuster SC, Miller W, Ratan A, et al. Complete Khoisan and Bantu genomes from southern Africa. Nature. 2010;463(7283):943-947.

68. Hollfelder N, Breton G, Sjӧdin P, Jakobsson M. The deep population history in Africa. Human Molecular Genetics. 2021;30(R1):R2-R10.

69. Hsieh P, Veeramah KR, Lachance J, et al. 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 Research. 2016;26(3):279-290.

70. Morris AG, Heinze A, Chan EK, Smith AB, Hayes VM. First ancient mitochondrial human genome from a prepastoralist southern African. Genome biology and evolution. 2014;6(10):2647-2653.

71. Lipson M, Ribot I, Mallick S, et al. Ancient West African foragers in the context of African population history. Nature. 2020;577(7792):665-670.

72. Barham L. Backed tools in Middle Pleistocene central Africa and their evolutionary significance. Journal of Human Evolution. 2002;43(5):585-603.

73. Taylor N. Across rainforests and woodlands: a systematic reappraisal of the Lupemban Middle Stone Age in Central Africa. Africa from MIS 6-2. 2016:273-299.

74. Grün R, Brink JS, Spooner NA, et al. Direct dating of Florisbad hominid. Nature. 1996;382(6591):500-501.

75. Dirks PH, Roberts EM, Hilbert-Wolf H, et al. The age of Homo naledi and associated sediments in the Rising Star Cave, South Africa. Elife. 2017;6:e24231.

76. Scerri EM, Blinkhorn J, Niang K, Bateman MD, Groucutt HS. Persistence of Middle Stone Age technology to the Pleistocene/Holocene transition supports a complex hominin evolutionary scenario in West Africa. Journal of Archaeological Science: Reports. 2017;11:639-646.

77. Niang K. The Early and Middle Stone Age of Senegal, West Africa.

78. De Weyer L. An Early Stone Age in Western Africa? Spheroids and polyhedrons at Ounjougou, Mali. Journal of Lithic Studies. 2017;4(1).

79. Wurz S. Southern and east African Middle Stone Age: geography and culture. Encyclopedia of global archaeology. 2014;2014:6890-912.

80. Harvati K, Stringer C, Grün R, Aubert M, Allsworth-Jones P, Folorunso CA. The later stone age calvaria from Iwo Eleru, Nigeria: Morphology and chronology. PLoS One. 2011;6(9):e24024.

81. Stojanowski CM. Iwo Eleru’s place among late Pleistocene and early Holocene populations of north and East Africa. Journal of human evolution. 2014;75:80-89.

82. Mendez FL, Krahn T, Schrack B, et al. An African American paternal lineage adds an extremely ancient root to the human Y chromosome phylogenetic tree. The American Journal of Human Genetics. 2013;92(3):454-459.

83. Shriner D, Rotimi CN. Genetic history of Chad. American journal of physical anthropology. 2018;167(4):804-812.

84. Gonder MK, Mortensen HM, Reed FA, de Sousa A, Tishkoff SA. Whole-mtDNA genome sequence analysis of ancient African lineages. Molecular biology and evolution. 2007;24(3):757-768.

85. Gomes V, Pala M, Salas A, et al. Mosaic maternal ancestry in the Great Lakes region of East Africa. Human genetics. 2015;134(9):1013-1027.

86. Gomes V, Sánchez-Diz P, Amorim A, Carracedo Á, Gusmão L. Digging deeper into East African human Y chromosome lineages. Human genetics. 2010;127(5):603-613.

87. Hassan HY, Underhill PA, Cavalli-Sforza LL, Ibrahim ME. Y-chromosome variation among Sudanese: restricted gene flow, concordance with language, geography, and history. American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists. 2008;137(3):316-323.

88. Lipson M, Sawchuk EA, Thompson JC, et al. Ancient DNA and deep population structure in sub-Saharan African foragers. Nature. 2022;603(7900):290-296.

89. Lachance J, Vernot B, Elbers CC, et al. Evolutionary history and adaptation from high-coverage whole-genome sequences of diverse African hunter-gatherers. Cell. 2012;150(3):457-469.

90. Skoglund P, Thompson JC, Prendergast ME, et al. Reconstructing prehistoric African population structure. Cell. 2017;171(1):59-71.

91. McDougall I, Brown FH, Fleagle JG. Stratigraphic placement and age of modern humans from Kibish, Ethiopia. nature. 2005;433(7027):733-736.

92. Vidal CM, Lane CS, Asrat A, et al. Age of the oldest known Homo sapiens from eastern Africa. Nature. 2022;601(7894):579-583.

93. Clark JD, Beyene Y, WoldeGabriel G, et al. Stratigraphic, chronological and behavioural contexts of Pleistocene Homo sapiens from Middle Awash, Ethiopia. Nature. 2003;423(6941):747-752.

94. Masao FT. Characterizing archaeological assemblages from eastern Lake Natron, Tanzania: results of fieldwork conducted in the area. African Archaeological Review. 2015;32(1):137-162.

95. McBrearty S, Tryon C. From Acheulean to middle stone age in the Kapthurin formation, Kenya. In: Transitions before the transition. Springer; 2006:257-277.

96. Van Peer P, Fullagar R, Stokes S, et al. The Early to Middle Stone Age transition and the emergence of modern human behaviour at site 8-B-11, Sai Island, Sudan. Journal of Human Evolution. 2003;45(2):187-193.

97. Cancellieri E, Bel Hadj Brahim H, Ben Nasr J, et al. A late Middle Pleistocene Middle Stone Age sequence identified at Wadi Lazalim in southern Tunisia. Scientific reports. 2022;12(1):1-12.

98. Salas A, Richards M, De la Fe T, et al. The making of the African mtDNA landscape. The American Journal of Human Genetics. 2002;71(5):1082-1111.

99. Silva M, Alshamali F, Silva P, et al. 60,000 years of interactions between Central and Eastern Africa documented by major African mitochondrial haplogroup L2. Scientific reports. 2015;5(1):1-13.

100. Soares P, Alshamali F, Pereira JB, et al. The expansion of mtDNA haplogroup L3 within and out of Africa. Molecular biology and evolution. 2012;29(3):915-927.

101. Kivisild T, Reidla M, Metspalu E, et al. Ethiopian mitochondrial DNA heritage: tracking gene flow across and around the gate of tears. The American Journal of Human Genetics. 2004;75(5):752-770.

102. \vCern\`y V, \vC’\i\vzková M, Poloni ES, Al-Meeri A, Mulligan CJ. Comprehensive view of the population history of A rabia as inferred by mt DNA variation. American Journal of Physical Anthropology. 2016;159(4):607-616.

103. Maca-Meyer N, González AM, Larruga JM, Flores C, Cabrera VM. Major genomic mitochondrial lineages delineate early human expansions. BMC genetics. 2001;2(1):1-8.

104. Metspalu M, Kivisild T, Metspalu E, et al. Most of the extant mtDNA boundaries in south and southwest Asia were likely shaped during the initial settlement of Eurasia by anatomically modern humans. BMC genetics. 2004;5(1):1-25.

105. Macaulay V, Hill C, Achilli A, et al. Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes. Science. 2005;308(5724):1034-1036.

106. Mellars P, Gori KC, Carr M, Soares PA, Richards MB. Genetic and archaeological perspectives on the initial modern human colonization of southern Asia. Proceedings of the National Academy of Sciences. 2013;110(26):10699-10704.

107. Yokoyama Y, Falgueres C, Lumley M. Direct dating of a Qafzeh proto-cro magnon skull by non destructive gamma-ray spectrometry. Comptes Rendus de l’Academie des Sciences Serie 2, Sciences de la Terre et des Planetes. 1997:773-779.

108. Schwarcz HP, Grün R, Vandermeersch B, Bar-Yosef O, Valladas H, Tchernov E. ESR dates for the hominid burial site of Qafzeh in Israel. Journal of Human Evolution. 1988;17(8):733-737.

109. Stringer C, Grün R, Schwarcz H, Goldberg P. ESR dates for the hominid burial site of Es Skhul in Israel. Nature. 1989;338(6218):756-758.

110. Mercier N, Valladas H, Bar-Yosef O, Vandermeersch B, Stringer C, Joron J-L. Thermoluminescence date for the Mousterian burial site of Es-Skhul, Mt. Carmel. Journal of Archaeological Science. 1993;20(2):169-174.

111. Lahr MM, Foley R. Multiple dispersals and modern human origins. Evolutionary Anthropology: Issues, News, and Reviews. 1994;3(2):48-60.

112. Tanaka M, Cabrera VM, González AM, et al. Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome research. 2004;14(10a):1832-1850.

113. Pagani L, Schiffels S, Gurdasani D, et al. Tracing the route of modern humans out of Africa by using 225 human genome sequences from Ethiopians and Egyptians. The American Journal of Human Genetics. 2015;96(6):986-991.

114. Beyin A. The Bab al Mandab vs the Nile-Levant: an appraisal of the two dispersal routes for early modern humans out of Africa. African Archaeological Review. 2006;23(1):5-30.

115. Richter J, Hauck T, Vogelsang R, Widlok T, Le Tensorer J-M, Schmid P. “Contextual areas” of early Homo sapiens and their significance for human dispersal from Africa into Eurasia between 200 ka and 70 ka. Quaternary International. 2012;274:5-24.

116. Shidrang S. Middle East Middle to Upper Paleolithic Transitional industries. Encyclopedia of Global Archaeology/ed C Smith-NY: Springer. 2014;7:4894-4907.

117. Armitage SJ, Jasim SA, Marks AE, Parker AG, Usik VI, Uerpmann H-P. The southern route “out of Africa”: evidence for an early expansion of modern humans into Arabia. Science. 2011;331(6016):453-456.

118. Marks AE. The Paleolithic of Arabia in an inter-regional context. In: The Evolution of Human Populations in Arabia. Springer; 2010:295-308.

119. Rose JI, Usik VI, Marks AE, et al. The Nubian complex of Dhofar, Oman: an African middle stone age industry in southern Arabia. PloS one. 2011;6(11):e28239.

120. Rodriguez-Flores JL, Fakhro K, Agosto-Perez F, et al. Indigenous Arabs are descendants of the earliest split from ancient Eurasian populations. Genome research. 2016;26(2):151-162.

121. Almarri MA, Haber M, Lootah RA, et al. The genomic history of the Middle East. Cell. 2021;184(18):4612-4625.

122. Groucutt HS, White TS, Scerri EM, et al. Multiple hominin dispersals into Southwest Asia over the past 400,000 years. Nature. 2021;597(7876):376-380.

123. Bretzke K, Preusser F, Jasim S, et al. Multiple phases of human occupation in Southeast Arabia between 210,000 and 120,000 years ago. Scientific reports. 2022;12(1):1-9.

124. Groucutt HS, Petraglia MD, Bailey G, et al. Rethinking the dispersal of Homo sapiens out of Africa. Evolutionary Anthropology: Issues, News, and Reviews. 2015;24(4):149-164.

125. Blinkhorn J, Groucutt HS, Scerri EM, Petraglia MD, Blockley S. Directional changes in Levallois core technologies between Eastern Africa, Arabia, and the Levant during MIS 5. Scientific reports. 2021;11(1):1-11.

126. Goder-Goldberger M, Gubenko N, Hovers E. “Diffusion with modifications”: Nubian assemblages in the central Negev highlands of Israel and their implications for Middle Paleolithic inter-regional interactions. Quaternary International. 2016;408:121-139.

127. Poznik GD, Xue Y, Mendez FL, et al. Punctuated bursts in human male demography inferred from 1,244 worldwide Y-chromosome sequences. Nature genetics. 2016;48(6):593-599.

128. Abu-Amero KK, Hellani A, González AM, Larruga JM, Cabrera VM, Underhill PA. Saudi Arabian Y-Chromosome diversity and its relationship with nearby regions. BMC genetics. 2009;10(1):1-9.

129. Cole CB, Zhu SJ, Mathieson I, Prüfer K, Lunter G. Ancient Admixture into Africa from the ancestors of non-Africans. bioRxiv. 2020.

130. Montinaro F, Pankratov V, Yelmen B, Pagani L, Mondal M. Revisiting the out of Africa event with a deep-learning approach. The American Journal of Human Genetics. 2021;108(11):2037-2051.

131. Kopp GH, Roos C, Butynski TM, et al. Out of Africa, but how and when? The case of hamadryas baboons (Papio hamadryas). Journal of Human Evolution. 2014;76:154-164.

132. Peer PV. Technological systems, population dynamics, and historical process in the MSA of Northern Africa. In: Africa from MIS 6-2. Springer; 2016:147-159.

133. Douze K, Delagnes A. The pattern of emergence of a Middle Stone Age tradition at Gademotta and Kulkuletti (Ethiopia) through convergent tool and point technologies. Journal of Human Evolution. 2016;91:93-121.

134. Mercier N, Valladas H, Froget L, et al. Thermoluminescence dating of a middle palaeolithic occupation at Sodmein Cave, Red Sea Mountains (Egypt). Journal of Archaeological Science. 1999;26(11):1339-1345.

135. White TD, Asfaw B, DeGusta D, et al. Pleistocene homo sapiens from middle awash, ethiopia. Nature. 2003;423(6941):742-747.

136. McDermott F, Stringer C, Grün R, Williams C, Din V, Hawkesworth C. New Late-Pleistocene uranium-thorium and ESR dates for the Singa hominid (Sudan). Journal of Human Evolution. 1996;31(6):507-516.

137. Yellen J, Brooks A, Helgren D, et al. The archaeology of aduma middle stone age sites in the Awash Valley, Ethiopia. PaleoAnthropology. 2005;10(25):e100.

138. Van Peer P, Vermeersch PM, Paulissen E. Chert quarrying, lithic technology and a modern human burial at the Palaeolithic site of Taramsa 1, Upper Egypt. Leuven university press; 2010.

139. Crevecoeur I. The Upper Paleolithic human remains of Nazlet Khater 2 (Egypt) and past modern human diversity. In: Modern Origins. Springer; 2012:205-219.

140. Maca-Meyer N, González AM, Pestano J, Flores C, Larruga JM, Cabrera VM. Mitochondrial DNA transit between West Asia and North Africa inferred from U6 phylogeography. BMC genetics. 2003;4(1):1-11.

141. Olivieri A, Achilli A, Pala M, et al. The mtDNA legacy of the Levantine early Upper Palaeolithic in Africa. Science. 2006;314(5806):1767-1770.

142. González AM, Larruga JM, Abu-Amero KK, Shi Y, Pestano J, Cabrera VM. Mitochondrial lineage M1 traces an early human backflow to Africa. BMC genomics. 2007;8(1):1-12.

143. Pennarun E, Kivisild T, Metspalu E, et al. Divorcing the Late Upper Palaeolithic demographic histories of mtDNA haplogroups M1 and U6 in Africa. BMC evolutionary biology. 2012;12(1):1-12.

144. Secher B, Fregel R, Larruga JM, et al. The history of the North African mitochondrial DNA haplogroup U6 gene flow into the African, Eurasian and American continents. BMC evolutionary biology. 2014;14(1):1-17.

145. Cruciani F, Trombetta B, Sellitto D, et al. Human Y chromosome haplogroup R-V88: a paternal genetic record of early mid Holocene trans-Saharan connections and the spread of Chadic languages. European Journal of Human Genetics. 2010;18(7):800-807.

146. Cruciani F, Santolamazza P, Shen P, et al. A back migration from Asia to sub-Saharan Africa is supported by high-resolution analysis of human Y-chromosome haplotypes. The American Journal of Human Genetics. 2002;70(5):1197-1214.

147. Mendez FL, Karafet TM, Krahn T, Ostrer H, Soodyall H, Hammer MF. Increased resolution of Y chromosome haplogroup T defines relationships among populations of the Near East, Europe, and Africa. Human biology. 2011;83(1):39-53.

148. Will M, Mackay A, Phillips N. Implications of Nubian-like core reduction systems in southern Africa for the identification of early modern human dispersals. PLoS One. 2015;10(6):e0131824.

149. Grine FE, Bailey RM, Harvati K, et al. Late Pleistocene human skull from Hofmeyr, South Africa, and modern human origins. Science. 2007;315(5809):226-229.

150. Crevecoeur I, Rougier H, Grine F, Froment A. Modern human cranial diversity in the Late Pleistocene of Africa and Eurasia: evidence from Nazlet Khater, Pe\cstera cu Oase, and Hofmeyr. American Journal of Physical Anthropology: The Official Publication of the American Association of Physical Anthropologists. 2009;140(2):347-358.

151. Garcea EA. Crossing deserts and avoiding seas: Aterian North African-European relations. Journal of Anthropological Research. 2004;60(1):27-53.

152. Hilbert YH, Crassard R, Rose JI, Geiling JM, Usik VI. Technological homogeneity within the Arabian Nubian Complex: Comparing chert and quartzite assemblages from central and southern Arabia. Journal of lithic Studies. 2016;3(2):411-437.

153. Westaway KE, Louys J, Awe R, et al. An early modern human presence in Sumatra 73,000-63,000 years ago. Nature. 2017;548(7667):322-325.

154. Clarkson C, Jacobs Z, Marwick B, et al. Human occupation of northern Australia by 65,000 years ago. Nature. 2017;547(7663):306-310.

155. Hammer MF, Woerner AE, Mendez FL, Watkins JC, Wall JD. Genetic evidence for archaic admixture in Africa. Proceedings of the National Academy of Sciences. 2011;108(37):15123-15128.

156. Durvasula A, Sankararaman S. Recovering signals of ghost archaic introgression in African populations. Science Advances. 2020;6(7):eaax5097.

157. Sankararaman S, Mallick S, Patterson N, Reich D. The combined landscape of Denisovan and Neanderthal ancestry in present-day humans. Current Biology. 2016;26(9):1241-1247.

158. Massilani D, Skov L, Hajdinjak M, et al. Denisovan ancestry and population history of early East Asians. Science. 2020;370(6516):579-583.

159. Hammer MF, Karafet T, Rasanayagam A, et al. Out of Africa and back again: nested cladistic analysis of human Y chromosome variation. Molecular biology and evolution. 1998;15(4):427-441.