The effect of the Neolithic expansion on European molecular diversity

We performed extensive and realistic simulations of the colonization process of Europe by Neolithic farmers, as well as their potential admixture and competition with local Palaeolithic hunter–gatherers. We find that minute amounts of gene flow between Palaeolithic and Neolithic populations should lead to a massive Palaeolithic contribution to the current gene pool of Europeans. This large Palaeolithic contribution is not expected under the demic diffusion (DD) model, which postulates that agriculture diffused over Europe by a massive migration of individuals from the Near East. However, genetic evidence in favour of this model mainly consisted in the observation of allele frequency clines over Europe, which are shown here to be equally probable under a pure DD or a pure acculturation model. The examination of the consequence of range expansions on single nucleotide polymorphism (SNP) diversity reveals that an ascertainment bias consisting of selecting SNPs with high frequencies will promote the observation of genetic clines (which are not expected for random SNPs) and will lead to multimodal mismatch distributions. We conclude that the different patterns of molecular diversity observed for Y chromosome and mitochondrial DNA can be at least partly owing to an ascertainment bias when selecting Y chromosome SNPs for studying European populations.

[1]  J. Biraben Essai sur l'évolution du nombre des hommes , 1979, Population.

[2]  Mathias Currat Effets des expansions des populations humaines en Europe sur leur diversité génétique , 2004 .

[3]  A. Gallay Genèse et diffusion de l'agriculture en Europe: agriculteurs, chasseurs, pasteurs , 2003 .

[4]  G. Barbujani,et al.  Genetic evidence on origin and dispersal of human populations speaking languages of the Nostratic macrofamily. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[5]  R J Mitchell,et al.  Y-chromosomal diversity in Europe is clinal and influenced primarily by geography, rather than by language. , 2000, American journal of human genetics.

[6]  S. Liu-Cordero,et al.  The discovery of single-nucleotide polymorphisms--and inferences about human demographic history. , 2001, American journal of human genetics.

[7]  H. Bandelt,et al.  In search of geographical patterns in European mitochondrial DNA. , 2002, American journal of human genetics.

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

[9]  M. Nordborg,et al.  Coalescent Theory , 2019, Handbook of Statistical Genomics.

[10]  R R Sokal,et al.  Indo-European origins: a computer-simulation test of five hypotheses. , 1995, American journal of physical anthropology.

[11]  D. Gronenborn A Variation on a Basic Theme: The Transition to Farming in Southern Central Europe , 1999 .

[12]  B. Sykes,et al.  Phylogeography of mitochondrial DNA in western Europe , 1998, Annals of human genetics.

[13]  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.

[14]  Francesc Calafell,et al.  A Recent Shift from Polygyny to Monogamy in Humans Is Suggested by the Analysis of Worldwide Y-Chromosome Diversity , 2003, Journal of Molecular Evolution.

[15]  E. Heyer,et al.  Variability of the genetic contribution of Quebec population founders associated to some deleterious genes. , 1995, American journal of human genetics.

[16]  A propos de travaux récents sur la néolithisation de l'Europe de l'Ouest , 1994 .

[17]  D. F. Roberts,et al.  The founding mitochondrial DNA lineages of Tristan da Cunha Islanders. , 1997, American journal of physical anthropology.

[18]  Lounès Chikhi,et al.  Estimating the impact of prehistoric admixture on the genome of Europeans. , 2004, Molecular biology and evolution.

[19]  P. Menozzi,et al.  Synthetic maps of human gene frequencies in Europeans. , 1978, Science.

[20]  Alberto Piazza,et al.  Simulation and Separation by Principal Components of Multiple Demic Expansions in Europe , 1986, The American Naturalist.

[21]  Newton E. Morton,et al.  The Neolithic Transition and the Genetics of Populations in Europe. , 2022 .

[22]  J. Bocquet-Appel,et al.  Traces paléoanthropologiques et archéologiques d'une transition démographique néolithique en Europe , 2003 .

[23]  R. Hudson Gene genealogies and the coalescent process. , 1990 .

[24]  G. Bertorelle,et al.  Genetics and the population history of Europe. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. Zvelebil The neolithic transition and the genetics of populations in Europe: By A. J. Ammerman and L. L. Cavalli-Sforza. 1984. 176 pp. tables, figs. Princeton, NJ: Princeton University Press. $25.00. ISBN 0 691 08357 6 , 1986 .

[26]  D. Labuda,et al.  Phylogenetic and familial estimates of mitochondrial substitution rates: study of control region mutations in deep-rooting pedigrees. , 2001, American journal of human genetics.

[27]  T. Price,et al.  Europe's First Farmers: Europe's first farmers: an introduction , 2000 .

[28]  L L Cavalli-Sforza,et al.  The genetic legacy of Paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective. , 2000, Nature Reviews Genetics.

[29]  Robert R. Sokal,et al.  Genetic evidence for the spread of agriculture in Europe by demic diffusion , 1991, Nature.

[30]  P. Gouyon,et al.  Effects of colonization processes on genetic diversity: differences between annual plants and tree species. , 2000, Genetics.

[31]  D. Balding,et al.  Handbook of statistical genetics , 2004 .

[32]  David Glenn Smith,et al.  Examining the Farming/Language Dispersal Hypothesis. , 2005 .

[33]  M. Otte,et al.  The Formation of the Aurignacian in Europe , 2000, Journal of Anthropological Research.

[34]  M. Richards The Neolithic invasion of Europe , 2003 .

[35]  L. Excoffier,et al.  Why hunter-gatherer populations do not show signs of pleistocene demographic expansions. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Christopher A. Edmonds,et al.  Mutations arising in the wave front of an expanding population. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Jobling,et al.  Y-chromosome mismatch distributions in Europe. , 2001, Molecular biology and evolution.

[38]  L. Excoffier Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite‐island model , 2004, Molecular ecology.

[39]  G. Barbujani,et al.  Y-chromosome polymorphisms and the origins of the European gene pool , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[40]  M. Zvelebil,et al.  Agricultural transition and Indo-European dispersals , 1988, Antiquity.

[41]  G. Collier Hunter-gatherer demography. , 1980, Science.

[42]  J. Zilhão Radiocarbon evidence for maritime pioneer colonization at the origins of farming in west Mediterranean Europe , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  A. Di Rienzo,et al.  Tracing European founder lineages in the Near Eastern mtDNA pool. , 2000, American journal of human genetics.

[44]  M. Milinkovitch,et al.  Genetic analysis of a successful repatriation programme: giant Galápagos tortoises , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[45]  A. Pérez-Lezaun,et al.  Geographic variation in human mitochondrial DNA control region sequence: the population history of Turkey and its relationship to the European populations. , 1996, Molecular biology and evolution.

[46]  Simcha Lev-Yadun,et al.  The Cradle of Agriculture , 2000, Science.

[47]  H. Bandelt,et al.  Paleolithic and neolithic lineages in the European mitochondrial gene pool. , 1996, American journal of human genetics.

[48]  R. Martin,et al.  The Cambridge encyclopedia of human evolution , 1994 .

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

[50]  A. Fix Gene frequency clines produced by kin-structured founder effects. , 1997, Human Biology: The Official Publication of the American Association of Anthropological Genetics.

[51]  J. Wakeley,et al.  Nonequilibrium migration in human history. , 1999, Genetics.

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

[53]  J. Bocquet-Appel,et al.  Neanderthal contraction and modern human colonization of Europe , 2000, Antiquity.

[54]  E. Heyer Mitochondrial and nuclear genetic contribution of female founders to a contemporary population in northeast Quebec. , 1995, American journal of human genetics.

[55]  V. Pascali,et al.  Clines of nuclear DNA markers suggest a largely neolithic ancestry of the European gene pool. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[56]  John Alroy,et al.  A Multispecies Overkill Simulation of the End-Pleistocene Megafaunal Mass Extinction , 2001, Science.

[57]  Robert L. Bettinger,et al.  Simulating the global human expansion in the LatePleistocene , 1995 .

[58]  S. Abbo,et al.  Archaeology. The cradle of agriculture. , 2000, Science.

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

[60]  P. Arias The Origins of the Neolithic Along the Atlantic Coast of Continental Europe: A Survey , 1999 .

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