Recovering the geographic origin of early modern humans by realistic and spatially explicit simulations.

Most genetic and archeological evidence argue in favor of a recent and unique origin of modern humans in sub-Saharan Africa, but no attempt has ever been made at quantifying the likelihood of this model, relative to alternative hypotheses of human evolution. In this paper, we investigate the possibility of using multilocus genetic data to correctly infer the geographic origin of humans, and to distinguish between a unique origin (UO) and a multiregional evolution (ME) model. We introduce here an approach based on realistic simulations of the genetic diversity expected after an expansion process of modern humans into the Old World from different possible areas and their comparison to observed data. We find that the geographic origin of the expansion can be correctly recovered provided that a large number of independent markers are used, and that precise information on past demography and potential places of origins is available. In that case, it is also possible to unambiguously distinguish between a unique origin and a multiregional model of human evolution. Application to a real human data set of 377 STR markers tested in 22 populations points toward a unique but surprising North African origin of modern humans. We show that this result could be due to ascertainment bias in favor of markers selected to be polymorphic in Europeans. A new estimation modeling this bias explicitly reveals that East Africa is the most likely place of origin for modern humans.

[1]  F. Balloux,et al.  Geography predicts neutral genetic diversity of human populations , 2005, Current Biology.

[2]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[3]  N. Takahata,et al.  The distribution of the ancestral haplotype in finite stepping‐stone models with population expansion , 2004, Molecular ecology.

[4]  T. Gage.  The comparative demography of primates: with some comments on the evolution of life histories. , 1998, Annual review of anthropology.

[5]  Paul Marjoram,et al.  Markov chain Monte Carlo without likelihoods , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  C. Stringer,et al.  On the reliability of recent tests of the Out of Africa hypothesis for modern human origins. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[7]  Lounès Chikhi,et al.  Y genetic data support the Neolithic demic diffusion model , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[8]  M. Wolpoff,et al.  Population bottlenecks and Pleistocene human evolution. , 2000, Molecular biology and evolution.

[9]  R. Hudson,et al.  Adjusting the focus on human variation. , 2000, Trends in genetics : TIG.

[10]  H. Vézina,et al.  New estimates of intergenerational time intervals for the calculation of age and origins of mutations. , 2000, American journal of human genetics.

[11]  Ian Tattersall,et al.  Out of Africa again ... and again , 1997 .

[12]  L. Excoffier,et al.  A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. , 1996, Genetics.

[13]  S. Gabriel,et al.  The Structure of Haplotype Blocks in the Human Genome , 2002, Science.

[14]  D. Balding,et al.  Approximate Bayesian computation in population genetics. , 2002, Genetics.

[15]  H. Harpending,et al.  Genetic perspectives on human origins and differentiation. , 2000, Annual review of genomics and human genetics.

[16]  M. Nachman,et al.  Genome scans of DNA variability in humans reveal evidence for selective sweeps outside of Africa. , 2004, Molecular biology and evolution.

[17]  S. Tishkoff,et al.  Global Patterns of Linkage Disequilibrium at the CD4 Locus and Modern Human Origins , 1996, Science.

[18]  Paul Mellars,et al.  Neanderthals and the modern human colonization of Europe , 2004, Nature.

[19]  J. Wall,et al.  When did the human population size start increasing? , 2000, Genetics.

[20]  M. Feldman,et al.  Genetic Structure of Human Populations , 2002, Science.

[21]  S. Pääbo,et al.  The genetical history of humans and the great apes , 2002, Journal of internal medicine.

[22]  D. F. Roberts,et al.  The History and Geography of Human Genes , 1996 .

[23]  G. McVean,et al.  A structured ancestral population for the evolution of modern humans. , 2004, Current opinion in genetics & development.

[24]  Scott M. Williams,et al.  Genetic analysis of African populations: human evolution and complex disease , 2002, Nature Reviews Genetics.

[25]  T. White,et al.  Pleistocene Homo sapiens from Middle Awash, Ethiopia , 2003, Nature.

[26]  Yungang He,et al.  Genetic evidence supports demic diffusion of Han culture , 2004, Nature.

[27]  L. Excoffier,et al.  Modern Humans Did Not Admix with Neanderthals during Their Range Expansion into Europe , 2004, PLoS biology.

[28]  L. Jorde,et al.  Ascertainment bias in estimates of average heterozygosity. , 1996, American journal of human genetics.

[29]  Estimating the Age of the Common Ancestor of Men from the ZFY Intron , 1996, Science.

[30]  L. Excoffier.  Human demographic history: refining the recent African origin model. , 2002, Current opinion in genetics & development.

[31]  Wen-Hsiung Li,et al.  Global patterns of human DNA sequence variation in a 10-kb region on chromosome 1. , 2001, Molecular biology and evolution.

[32]  M. Wolpoff,et al.  Multiregional, not multiple origins. , 2000, American journal of physical anthropology.

[33]  M. Feldman,et al.  The application of molecular genetic approaches to the study of human evolution , 2003, Nature Genetics.

[34]  K. Hawkes,et al.  African populations and the evolution of human mitochondrial DNA. , 1991, Science.

[35]  M. Feldman,et al.  Population growth of human Y chromosomes: a study of Y chromosome microsatellites. , 1999, Molecular biology and evolution.

[36]  S. Pääbo,et al.  Mitochondrial genome variation and the origin of modern humans , 2000, Nature.

[37]  L. Excoffier,et al.  Intra-deme molecular diversity in spatially expanding populations. , 2003, Molecular biology and evolution.

[38]  Alberto Piazza,et al.  The History and Geography of Human Genes: Abridged paperback Edition , 1996 .

[39]  Chris Stringer,et al.  Modern human origins: progress and prospects. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  N. Takahata,et al.  Testing multiregionality of modern human origins. , 2001, Molecular biology and evolution.

[41]  Laurent Excoffier,et al.  splatche: a program to simulate genetic diversity taking into account environmental heterogeneity , 2004 .

[42]  M. Stoneking,et al.  Genetic Evidence for the Demic Diffusion of Agriculture to India , 2004, Science.

[43]  J. Gulcher,et al.  A populationwide coalescent analysis of Icelandic matrilineal and patrilineal genealogies: evidence for a faster evolutionary rate of mtDNA lineages than Y chromosomes. , 2003, American journal of human genetics.

[44]  M. Hammer,et al.  Heterogeneous Patterns of Variation Among Multiple Human X-Linked Loci , 2004, Genetics.

[45]  T. Sluckin,et al.  Modelling Paleoindian dispersals , 1998 .