Out of Eden: The Peopling of the World

by Oppenheimer, Stephen

  27. different frequencies outside Africa (of DNA variants of functioning nuclear genes): For instance beta globin RFLP haplotypes see Wainscoat et al. (1986) ‘Evolutionary relationships of human populations from an analysis of nuclear DNA polymophisms’ Nature 319: 491–3. For beta globin genes see Harding, R.M. et al. (1997) ‘Archaic African and Asian lineages in the genetic ancestry of modern humans’ American Journal of Human Genetics 60: 772–89. For GM system see Walter, H. (1998) Populationsgenetik der Blutgruppensystems des Menschen (E. Schweizer’bartsche Verlagsbuchhandlung, Stuttgart). For X chromosome see Harris, E.E. and Hey, J. (1999) ‘X chromosome evidence for ancient human histories’ Proceedings of the National Academy of Sciences USA 96: 3320–24. For dystrophin gene see Labuda, D. et al. (2000) ‘Archaic lineages in the history of modern humans’ Genetics 156: 799–808. The absence of specific extra packets: e.g. Alu insertions, Stoneking et al. (1997) op. cit.

  28. See especially Stoneking et al. (1997) op. cit.; Mountain, J.L. and Cavalli-Sforza, L.L. (1994) ‘Inference of human evolution through cladistic analysis of nuclear DNA restriction polymorphisms’ Proceedings of the National Academy of Sciences USA 91: 6515–19. But also: (a) African beta globin RFLP haplotypes ‘– + – +’ and ‘– – +’ are found only in Oceania, Wainscoat et al., op. cit.; (b) African beta globin haplotypes C3 and A2 are found only in Papua New Guinea and Vanuatu, Harding et al. (1997) op. cit.; (c) Gm alleles 7 (and 6) are closest to African 8 and commonest in Sahul, while allele 7 is specific to Sahul – Table 5.2 of Propert, D. (1989) ‘Immunoglobin allotypes’, in A.V.S. Hill and S.W. Serjeantson (eds) The Colonization of the Pacific: A Genetic Trail (Clarendon Press, Oxford) pp. 194–214; (d) X chromosome: A, B, O, and D are haplogroups shared between Africa and the rest of the world, Sahul has all haplogroups except B – Kaessmann, H. et al. (1999) ‘DNA sequence variation in a non-coding region of low recombination on the human chromosome’ Nature Genetics 22: 78–81; (e) Chromosome 21: Oceania shares more haplotypes with Africa than does any other region – Li Jin et al., op. cit.

  29. This paragraph, see: Fig. 2 in Stoneking et al. (1997) op. cit., southern Arabia being represented in this study by the United Arab Emirates. See also Fig. 2 in Watkins et al. (2001) op. cit.

  30. although some of these markers: i.e. non-African ‘L3*’, Richards M. et al. (2003) ‘Extensive female-mediated gene flow from sub-Saharan Africa into Near Eastern Arab populations’ American Journal of Human Genetics 72: 1058–64. arrived from Africa more recently: ancient Exodus types would be non-African and derived from L3, e.g. non-African L3*, M*, and N* super-clans; recent intrusions would include the ‘older’ specific African branches L1, L2, and African-specific L3 subgroups (for definitions/nomenclature see ibid. and Richards and Macaulay (2000) op. cit.; see also the mtDNA tree at end of this book Fig 8.2). What is clear is that, unlike North Africans and Levantines, the Hadramaut also carry roots and most of the primary branches of the Eurasian super-clans M and N (namely M*, M1, M2, M7, D, N1b, R1, R2, X, F, Pre-HV, HV1, H, U*,U2, U5, U7, J*, J1, J1b, J2, T*, T1, and K; data from Richards et al. (2003) op. cit. a higher rate of the African ancestral types: See Table 1 and Fig. 2 in Watkins et al. (2001) op. cit.

  31. shares some ancient mtDNA links: i.e. both U/HV haplogroups as well as M haplogroup, e.g. U2i, U7, and Pre-HV, as well as M types: M*, M1, M2b, M4, and M-C. See Kivisild, T. et al. (1999a) ‘The place of the Indian mitochondrial DNA variants in the global network of maternal lineages and the peopling of the Old World’ in S.S. Papiha et al. (eds) Genomic Diversity: Applications in Human Population Genetics (Kluwer Academic/Plenum, New York) pp. 135–52. They have an African Y-chromosome marker: Hammer YAP+ Haplotype 5a defined by PN1, Mehdi, S.Q. et al. (1999) ‘The origins of Pakistani populations: Evidence from Y chromosome markers’ in S.S. Papiha et al. (eds) Genome Diversity: Applications in Human Populations (Kluwer Academic/Plenum, New York) pp. 83–91. Hammer argues that the presence of this haplotype (and its ancestral type) in Saudi Arabia, the United Arab Emirates, and Iran (and its virtual absence from Ethiopia) supports his view that the YAP+ mutation originally occurred outside Africa – Altheide, T.K. and Hammer, M.F. (1997) ‘Evidence for a possible Asian Origin of YAP+ Y chromosomes’ American Journal of Human Genetics 61: 462–6. I agree, although the conventional opposite view – that this represents a more recent introduction by the slave trade from sub-Saharan Africa – is still possible. Another unique Y-chromosome marker appears outside Africa only in this region: Underhill Haplotype 12, Underhill et al., op. cit. an early branch off the Out-of-Africa Adam: Underhill Haplotypes 90–91, ibid.; consensus haplogroup L in Kivisild et al (2003) op. cit. and Wells R.S. et al. (2001) ‘The Eurasian heartland: a continental perspective on Y-chromosome diversity’ Proceedings of the National Academy of Sciences USA 98: 10244–9.

  32. greatest genetic diversity of Rohani’s western daughters: Rohani types in an Iraqi sample: H* (10), H(1–51) (17), HV* (8), HV1 (2), HV1a, HV1b, J* (6), J1 (3), J1b (5), J2, K* (2), K2 (2), Pre-HV (5), R* (3), R1, R2, T* (3), T1 (5), T2, U* (5), U1a, U2 (2), U3 (5), U3a, U4 (2), U5a1a, U6a*, U7 (3), U7a (n = 116). unclassified root genetic types: in the foregoing list, an asterisk ‘*’ indicates an unclassified paraphyletic haplotype. Data from Richards, M. et al. (2000) ‘Tracing European founder lineages in the Near Eastern mtDNA pool’ American Journal of Human Genetics 67: 1251–76.

  33. for Rohani’s Indian granddaughter U2i to be of a similar age: For a comparison of the diversity and age of Indian U types see Kivisild et al. (1999a) op. cit.; Kivisild, T. et al. (1999b) ‘Deep common ancestry of Indian and Western-Eurasian mitochondrial DNA lineages’ Current Biology 9: 1331–4. several early non-African Y-chromosome genetic groups: in particular haplogroups 3 and 9, in: Quintana-Murci, L. et al. (2001) ‘Y-chromosome lineages trace diffusion of people and languages in Southwestern Asia’ American Journal of Human Genetics 68: 537–42.

  34. Hadramaut . . . ratio . . . 5:1 Nasreen to Manju: (Hadramaut see above, and note 30 – N diversity also higher than M) – data from Richards et al. (2003) op. cit. consistent with the view that Nasreen originated farther west than Manju, in the Gulf region: the node type for N has not been found in India, Europe, or the Levant, although N* types have been found in the Yemen and Tashkent – data from Thomas, M.G. et al. (2002) ‘Founding mothers of Jewish communities: Geographically separated Jewish groups were independently founded by very few female ancestors’ American Journal of Human Genetics 70: 1411–20. decreases to 2:1 in the far-western states: in the north-central/north-eastern regions of the Punjab and Uttar Pradesh the ratio is 1:1, while in Andhra Pradesh on the east coast M outnumbers N by 2:1, data from Kivisild et al. (1999a,b) op. cit. Manju dominates at 5:1: data from ibid.

  35. In Tibet, East Asian N subgroups A, B, and F constitute 31.5%, and East Asian M subgroups: C, D, E, and G 36%, Torroni, A. et al. (1994) ‘Mitochondrial DNA analysis in Tibet: Implications for the origins of the Tibetan population and its adaptaton to high altitude’ American Journal of Physical Anthropology 93: 189–99.

  36. Bulbeck (1999) op. cit.

  37. Much of this paragraph draws on Kivisild et al. (1999a, 2003) op. cit. Manju achieves her greatest diversity and antiquity in India: Kivisild et al. (1999a,b, 2003) op. cit. M2, even dates to 73,000 years ago: Kivisild et al (2003) op. cit. M2 is strongly represented in the Chenchu: ibid. strong reasons for placing Manju’s birth in India: It has been argued that M might have been born farther west, in Ethiopia, on the basis of a single sub-branch, ‘M1’, found there with high diversity – Quintana-Murci, L. et al. (1999) ‘Genetic evidence for an early exit of Homo sapiens sapiens from Africa through eastern Africa’ Nature Genetics 23: 437–41. Closer inspection of Ethiopia shows no non-M1 branches or M root (underived), nor her sister N’s roots. Further, when M1 is dated in Ethiopia on the basis of local diversity, it turns out that her age is only about 12,500 years – Kivisild, T. et al. ‘A likely post-LGM impact of Western Asian maternal lineages to Eastern Africans’ abstract, Cold Spring Ha
rbor Symposium on ‘Human Origins and Disease’ October 2000. This means that the M1’s age in Ethiopia is younger than the last glaciation, and she is therefore more likely to be a single re-entrant from South Asia.

  38. a scattering of other Europa clans: U1, U3 – U6; see: Kivisild et al. (2003) op. cit. a scattering of her first-generation daughters: X, I, and, in particular, W – Kivisild et al. (1999a,b, 2003) op. cit.

  39. mother to most Westerners: including the HV and JT clans, Kivisild, T. et al. (1999a,b) op. cit., Kivisild et al. (2002) ‘The emerging limbs and twigs of the East Asian mtDNA tree’ Molecular Biology and Evolution 19(10): 1737–51, Kivisild et al. (2003) op. cit. two Far Eastern daughters: Haplogroups F and B, see the full gene network in Richards and Macaulay (2000) op. cit. 73,000 years ago: Kivisild et al. (2003) op. cit.

  40. Kivisild et al. (2003) op. cit.

  41. [Out-of-Africa] Adam’s root line [absent] outside Africa: would be defined as ‘M168*’ in Underhill et al., op. cit., but all members of the M168 clade belong to one of the three branches. Cain, Abel, and Seth: respectively M130 (C or RPS4Y), M1 (D’E or YAP), and M89 (or F), ibid. These three lines and their descendants are labelled by at least six different numbering systems by different scientists, so we need to give them some recognizable and consistent names. I have chosen to use the marker system (except when referring to individual haplotypes defined in cited papers in the endnotes) and haplotypes identified in The Y Chromosome Consortium (2002) ‘A nomenclature system for the tree of human Y-chromosomal binary haplogroups’ Genome Research 12: 339–48. In the main text, as shown, I name the main branches, generally using the consensus lettering as a cue for the first letter – except in the case of Abel and Seth.

  42. One of these three root branches, C (or RPS4Y): M130. For the label ‘Consensus type C/Cain’, see the explanation above. Cain is present at an even rate: Kivisild et al. (2003) op. cit. F nearly exclusively non-African with the exception of several root types: Haplotypes 50, 58, and 71 (Underhill et al., op. cit.); Haplotype 71 is the root M89/Seth type (Consensus type F) and also appears infrequently in Sudan and Ethiopia (Haplotypes 58 and 71 are also found in India). All three haplotypes are found in Morocco (Underhill et al., op. cit.), which has a large European genetic admixture of recent origin that explains this exception. Admixture: See Rando, J.C. et al. (1998) ‘Mitochondrial DNA analysis of Northwest African populations reveals genetic exchanges with European, near-Eastern, and sub-Saharan populations’ Annals of Human Genetics 62: 531–50. For the label ‘F/Seth’ in place of M89, see the explanation in note 41. high rates in Australia and New Guinea: Kayser, M. et al. (2001) ‘Independent histories of human Y chromosomes from Melanesia and Australia’ American Journal of Human Genetics 68: 173–90. He accounts for 95–98 per cent of Indian male lines: Fig. 3 in Kivisild et al. (2003) op. cit.

  43. Two of these are offspring of group K, or Krishna: 2 Krishna sons Consensus classified respectively as L1 (which is commonest in Tamil Nadu in South India – Wells et al., op. cit. – and is also found in the Greater Andaman Islands – Chapter 5 note 44) and R2 (which is commonest farther to the east, in West Bengal) see Kivisild et al. (2003) op. cit. third is a first-degree branch from Seth: defined by M69 and including mainly Consensus subgroup H1, but also H* and H2, Kivisild et al. (2003) op. cit. three types feature strongly: Kivisild et al. (2003) op. cit.; Wells et al., op. cit. a root Seth type in a quarter of their population, restricted to the Indian subcontinent: F* in Kivisild et al. (2003) op. cit.

  44. another view of out-of-Africa: Underhill, P.A. et al. (2001a) ‘The phylogeography of Y-chromosome binary haplotypes and the origins of modern human populations’ Annals of Human Genetics 65: 43–62. This type is M17: data from Kivisild et al. (2003) op. cit.; Quintana-Murci, L. et al.; Wells et al., op. cit.

  45. a small, deep, early Asian branch: ‘Asian YAP’: Consensus type D, Haplotypes 40–43, nodal haplotype 40, Underhill haplogroup IV (Underhill et al. (2000) op. cit) but see also Underhill et al. (2001a) op. cit. The other, western YAP branch: Consensus type E, Underhill haplotypes 19–39. See also above, note 31 - (Mehdi, S.Q. et al., op. cit.) commonest back in Africa: Underhill haplotypes 19–30; but see also Underhill et al. (2001a) op. cit., where they are also defined by PN2 and PN1 (Haplotypes 20–27). characteristic of the Middle East: Underhill haplotypes 31–39; but see also Underhill et al. (2001a) op. cit., where they are further defined by PN2 M35 (Underhill (2001) Haplotypes 29–38); YAP+ types in general are notably lacking in the Khoisan, except for a small number of the two commonest haplotypes with the PN2 marker. This could be consistent with an ancient YAP intrusion to Africa from the Middle East (as per Hammer’s back-to-Africa YAP hypothesis) with subsequent expansion during the Neolithic and only minimal intrusion to hunter-gatherer populations.

  46. e.g. Underhill et al. (2001a) op. cit.

  47. i.e. mtDNA types: M1, and pre-HV; Y chromosome types: YAP+ Underhill haplotypes, especially 19–30.

  48. Trask, R.L. (1996) Historical Linguistics (Arnold, London) p. 377.

  49. Kivisild et al. (2000) op. cit.

  50. his complete absence from India: Kivisild et al. (2003) op. cit.; Wells et al., op. cit. [Central] Asian YAP at rates of 3–6 per cent: Wells et al., op. cit. much lower rates there [India] than in Central Asia: Kivisild et al. (2003), op. cit.; Wells et al., op. cit.

  51. in Australia he is the dominant line: Kayser, M. et al. (2001) op. cit. Eastern Indonesia . . . the least changed or root Cain type: Underhill, P.A. et al. (2001b) ‘Maori origins, Y chromosome haplotypes and implications for human history in the Pacific’ Human Mutation 17: 271–80. From which the unique Australian type is derived: Haplotypes 2 (M210) in Underhill et al. (2001b) op. cit. other place . . . root Cain type is found is India . . . Australoid tribal groups: C* in Fig. 3 in Kivisild et al. (2003) op. cit. On the neighbouring island of New Guinea: Capelli, C. et al. (2001) ‘A predominantly indigenous paternal heritage for the Austronesian-speaking peoples of insular Southeast Asia and Oceania’ American Journal of Human Genetics 68: 432–3; Kayser, M. et al. (2000) ‘Melanesian origin of Polynesian Y chromosomes’ Current Biology 10: 1237–46; Haplotype 3 (M38) in Underhill et al. (2001b) op. cit. A breakdown of Cain frequency: Kayser, M. et al. (2000, 2001) op. cit.; Karafet, T.M. et al. (1999) ‘Ancestral Asian source(s) of New World Y-chromosome founder haplotypes’ American Journal of Human Genetics 64: 817–31. Asian types mainly belong to one derived clan: M217 (Consensus group C3), Underhill et al. (2001b) op. cit.

  52. one of the two remaining founding male types: Consensus type F/Seth = M89 base in Kayser et al. (2001) op. cit. Seth in his ancestral or root form in all these areas: the black shaded areas in Fig. 1 of ibid. Krishna [at 30%] throughout Southeast Asia and Australia: the gray shaded areas in Fig. 1 of ibid. The third root Y line, the Asian YAP: Karafet et al. (1999) op. cit.; Bing Su et al. (1999) ‘Y-chromosome evidence for a northward migration of modern humans into Eastern Asia during the last ice age’ American Journal of Human Genetics 65: 1718–24.

  53. Root and branch for Cain, Seth, and Seth’s genetic sons and grandsons [in Pakistan and/or India]: Consensus type C/Cain (RPS4Y): Haplotype 46; Consensus type F/Seth (M89): Haplotype 71; F/Seth’s derivatives: M89/M172 Haplotypes 56–58, 60, 61, and 64; M89/M52 Haplotypes 65, 67, and 68; M89/M9 Haplotype 87; M89/M9/M175/M122 Haplotypes 78 and 79; M89/M9/M70 Haplotype 88; M89/M9/M147 Haplotype 89; M89/M9/M11 Haplotypes 90 and 91; M89/M9/M45 Haplotypes 111 and 113; M89/M9/M45/M173 Haplotype 104; M89/M9/M45/M173/M17 Haplotypes 108 and 106 – all in Underhill et al. (2000) op. cit. several unique [western] YAP types: Haplotypes 31 and 34, Underhill et al. (2000) op. cit. In addition to these unique YAP haplotypes which may support the Hammer hypothesis of YAP outside Africa, there are representatives from an African clan, Haplotype 12, found in India and Pakistan.

  54. Fig. 2 in Metspalu, E. et al. (1999) ‘The Trans-Caucasus and the expansion of the Caucasoid-specific mitochondrial DNA’ in S.S. Papiha, et al. (eds), Genomic Diversity: Applications
in Human Population Genetics (Kluwer Academic/Plenum, New York) pp. 121–34.

  Chapter 5

  1. Dunbar, R.I.M. (1992) ‘Neocortex size as a constraint on group size in primates’ Journal of Human Evolution 20: 469–93.

  2. Jablonski, N. and Chaplin, G. (2000) ‘The evolution of human skin coloration’ Journal of Human Evolution 39: 57–106.

  3. selective pressure to remain dark-skinned: e.g. seen as differential selection at the MC1R locus, which explains a substantial phenotypic component of melanin production – Harding, R. et al. (2000) ‘Evidence for variable selective pressures at MC1R’ American Journal of Human Genetics 66: 1351–61. tuned to local relative levels of ultraviolet light: Jablonski and Chaplin op. cit.