Out of Africa again and again

Abstract

The publication of a haplotype tree of human mitochondrial DNA variation in 1987 provoked a controversy about the details of recent human evolution that continues to this day. Now many haplotype trees are available, and new analytical techniques exist for testing hypotheses about recent evolutionary history using haplotype trees. Here I present formal statistical analysis of human haplotype trees for mitochondrial DNA, Y-chromosomal DNA, two X-linked regions and six autosomal regions. A coherent picture of recent human evolution emerges with two major themes. First is the dominant role that Africa has played in shaping the modern human gene pool through at least two—not one—major expansions after the original range extension of Homo erectus out of Africa. Second is the ubiquity of genetic interchange between human populations, both in terms of recurrent gene flow constrained by geographical distance and of major population expansion events resulting in interbreeding, not replacement.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: A new model of recent human evolution.
Figure 2: The distributions for the ages of the youngest clade contributing to a significant inference of gene flow constrained by isolation by distance at the highest nesting level for the genes MX1, PDHA1, EDN and ECP, and at intermediate nesting levels for the β-globin (β-Hb) locus and the Xq13.3 region.
Figure 3: The distributions for the ages of the youngest clade contributing to a significant inference of a population range expansion for mtDNA, Y-DNA, MC1R, MS205, and the β-globin (β-Hb) locus.

References

  1. 1

    Relethford, J. H. Genetics and the Search for Modern Human Origins (Wiley, New York, 2001).

  2. 2

    Stoneking, M. & Soodyall, H. Human evolution and the mitochondrial genome. Curr. Opin. Genet. Dev. 6, 731–736 (1996).

  3. 3

    Wolpoff, M. H., Hawks, J. & Caspari, R. Multiregional, not multiple origins. Am. J. Phys. Anthropol. 112, 129–136 (2000).

  4. 4

    Weidenreich, F. Apes, Giants, and Man (Univ. Chicago Press, Chicago, 1946).

  5. 5

    Cann, R. L., Stoneking, M. & Wilson, A. C. Mitochondrial DNA and human evolution. Nature 325, 31–36 (1987).

  6. 6

    Vigilant, L., Stoneking, M., Harpending, H., Hawkes, K. & Wilson, A. C. African populations and the evolution of human mitochondrial DNA. Science 253, 1503–1507 (1991).

  7. 7

    Maddison, D. R. African origin of human mitochondrial DNA reexamined. Syst. Zool. 40, 355–363 (1991).

  8. 8

    Templeton, A. R. Human origins and analysis of mitochondrial DNA sequences. Science 255, 737 (1992).

  9. 9

    Ingman, M., Kaessmann, H., Pääbo, S. & Gyllensten, U. Mitochondrial genome variation and the origin of modern humans. Nature 408, 708–713 (2000).

  10. 10

    Sykes, B., Leiboff, A., Low-Beer, J., Tetzner, S. & Richards, M. The origins of the Polynesians: an interpretatioon from mitochondrial lineage analysis. Am. J. Hum. Genet. 57, 1463–1475 (1995).

  11. 11

    Torroni, A. et al. Asian affinities and continental radiation of the four founding native American mtDNAs. Am. J. Hum. Genet. 53, 563–590 (1993).

  12. 12

    Torroni, A. et al. mtDNA variation of aboriginal Siberians reveals distinct genetic affinities with Native Americans. Am. J. Hum. Genet. 53, 591–608 (1993).

  13. 13

    Hammer, M. F. et al. Out of Africa and back again: Nested cladistic analysis of human Y chromosome variation. Mol. Biol. Evol. 15, 427–441 (1998).

  14. 14

    Harris, E. E. & Hey, J. X. Chromosome evidence for ancient human histories. Proc. Natl Acad. Sci. USA 96, 3320–3324 (1999).

  15. 15

    Kaessman, H., Heißig, F., Haeseler, A. V. & Pääbo, S. DNA sequence variation in a non-coding region of low recombination on the human X chromosome. Nature Genet. 22, 78–81 (1999).

  16. 16

    Harding, R. M. et al. Archaic African and Asian lineages in the genetic ancestry of modern humans. Am. J. Hum. Genet. 60 772–789 (1997).

  17. 17

    Jin, L. et al. Distribution of haplotypes from a chromosome 21 region distinguishes multiple prehistoric human migrations. Proc. Natl Acad. Sci. USA 96, 3796–3800 (1999).

  18. 18

    Rana, B. K. et al. High polymorphism at the human melanocortin 1 receptor locus. Genetics 151, 1547–1557 (1999).

  19. 19

    Rogers, E. J., Shone, A. C., Alonso, S., May, C. A. & Armour, J. A. L. Integrated analysis of sequence evolution and population history using hypervariable compound haplotypes. Hum. Mol. Genet. 9, 2675–2681 (2000).

  20. 20

    Zhang, J. & Rosenberg, H. F. Sequence variation at two eosinophil-associated ribonuclease loci in humans. Genetics 156, 1949–1958 (2000).

  21. 21

    Templeton, A. R., Routman, E. & Phillips, C. Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the Tiger Salamander, Ambystoma tigrinum. Genetics 140, 767–782 (1995).

  22. 22

    Posada, D., Crandall, K. A. & Templeton, A. R. GeoDis: a program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9, 487–488 (2000).

  23. 23

    Templeton, A. R. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol. Ecol. 7, 381–397 (1998).

  24. 24

    Bernatchez, L. The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nested clade, and mismatch analyses of mitochondrial DNA variation. Evolution 55, 351–379 (2001).

  25. 25

    Gomez, A., Carvalho, G. R. & Hunt, D. H. Phylogeography and regional endemism of a passively dispersing zooplankter: mitochondrial DNA variation in rotifer resting egg banks. Proc. R. Soc. Lond. B 267, 2189–2197 (2000).

  26. 26

    Nielson, M., Lohman, K. & Sullivan, J. Phylogeography of the tailed frog (Ascaphus truei): Implications for the biogeography of the Pacific Northwest. Evol. 55, 147–160 (2001).

  27. 27

    Turner, T. F., Trexler, J. C., Harris, J. L. & Haynes, J. L. Nested cladistic analysis indicates population fragmentation shapes genetic diversity in a freshwater mussel. Genetics 154, 777–785 (2000).

  28. 28

    Templeton, A. R., Crandall, K. A. & Sing, C. F. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633 (1992).

  29. 29

    Posada, D. TCS 1.06 (Provo, Utah, 2000); available at http://bioag.byu.edu/zoology/crandall_lab/tcs.htm.

  30. 30

    Crandall, K. A. & Templeton, A. R. Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969 (1993).

  31. 31

    Templeton, A. R. in Conceptual Issues in Modern Human Origins Research (eds Clark, G. A. & Willermet, C. M.) 329–360 (Aldine de Gruyter, New York, 1997).

  32. 32

    Templeton, A. R. Human races: A genetic and evolutionary perspective. Am. Anthropol. 100, 632–650 (1998).

  33. 33

    Templeton, A. R. Using phylogeographic analyses of gene trees to test species status and processes. Mol. Ecol. 10 779–791 (2001).

  34. 34

    Excoffier, L. & Langaney, A. Origin and differentiation of human mitochondrial DNA. Am. J. Human. Genet. 44, 73–85 (1989).

  35. 35

    Excoffier, L. Evolution of human mitochondrial DNA: evidence for departure from a pure neutral model of populations at equilibrium. J. Mol. Evol. 30, 125–139 (1990).

  36. 36

    Donnelly, P. & Tavare, S. Coalescents and genealogical structure under neutrality. Annu. Rev. Genet. 29, 401–421 (1995).

  37. 37

    Takahata, N., Lee, S.-H. & Satta, Y. Testing multiregionality of modern human origins. Mol. Biol. Evol. 18, 172–183 (2001).

  38. 38

    Haile-Selassie, Y. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412, 178–181 (2001).

  39. 39

    Pickford, M. & Senut, B. The geological and faunal context of the Late Miocene hominid remains from Lukeino, Kenya. C.R. Acad. Sci. IIA 332, 145–152 (2001).

  40. 40

    Templeton, A. R. The “Eve” hypothesis: a genetic critique and reanalysis. Am. Anthropol. 95, 51–72 (1993).

  41. 41

    Alonso, S. & Armour, J. A. L. A highly variable segment of human subterminal 16p reveals a history of population growth for modern humans outside Africa. Proc. Natl. Acad. Sci. USA 98, 864–869 (2001).

  42. 42

    Rannala, B. & Bertorelle, G. Using linked markers to infer the age of a mutation. Hum. Mutat. 18, 87–100 (2001).

  43. 43

    Gabunia, L. et al. Earliest Pleistovene hominid cranial remains from Dmanisi, Republic of Georgia: Taxonomy, geological setting, and age. Science 288, 1019–1025 (2000).

  44. 44

    Aguirre, E. & Carbonell, E. Early human expansions into Eurasia: The Atapuerca evidence. Quat. Int. 75, 11–18 (2001).

  45. 45

    Bar-Yosef, O. & Belfer-Cohen, A. From Africa to Eurasia—early dispersals. Quat. Int. 75, 19–28 (2001).

  46. 46

    Hou, Y. M. et al. Mid-Pleistocene Acheulean-like stone technology of the Bose basin, South China. Science 287, 1622–1626 (2000).

  47. 47

    Saragusti, I. & Goren-Inbar, N. The biface assemblage from Gesher Benot Ya'aqov, Israel: illuminating patterns in “Out of Africa” dispersal. Quat. Int. 75, 85–89 (2001).

  48. 48

    Otte, M. in Archaeogenetics: DNA and the Population Prehistory of Europe (eds Renfrew, C. & Boyle, K.) 41–44 (Univ. Cambridge, Cambridge, 1999).

  49. 49

    Smith, F. H., Falsetti, A. B. & Donnelly, S. M. Modern human origins. Yb. Physical Anthrop. 32, 35–68 (1989).

  50. 50

    Wolpoff, M., Thorne, A. G., Smith, F. H., Frayer, D. W. & Pope, G. G. in Origins of Anatomically Modern Humans (eds Nitecki, M. H. & Nitecki, D. V.) 175–200 (Plenum, New York, 1994).

Download references

Acknowledgements

I thank J. Brisson, J. Hess, R. Koch, M. Kramer, R. Robertson and J. Strasburg for suggestions on an earlier draft of this manuscript. I also thank E. Trinkhaus and J. Relethford for their reviews. This work was supported in part by a Burroughs Wellcome Fund Innovation Award in Functional Genomics.

Author information

Supplementary information

Overview and content listing for all other Supplementary Information files (PDF 4 kb)

Nested clade method of phylogeographic analysis (PDF 4 kb)

GeoDis v2.0. documentation (PDF 55 kb)

Geodis inference key (PDF 6 kb)

Geodis ECP date set analysis (PDF 6 kb)

Geodis EDN data set analysis (PDF 5 kb)

Geodis MC1R data set analysis (PDF 6 kb)

Geodis mtDNA data set analysis (PDF 27 kb)

Geodis PDHA data set analysis (PDF 9 kb)

Geodis MS205a data set analysis (PDF 11 kb)

Geodis MS205b data set analysis (PDF 11 kb)

Geodis MS205c data set analysis (PDF 10 kb)

Supplementary Information

Supplementary Information (PDF 176 kb)

Rights and permissions

Reprints and Permissions

About this article

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.