Pleistocene Mitochondrial Genomes Suggest a Single Major Dispersal of Non-Africans and a Late Glacial Population Turnover in Europe

Abstract

How modern humans dispersed into Eurasia and Australasia, including the number of separate expansions and their timings, is highly debated [1Scally A. Durbin R. Revising the human mutation rate: implications for understanding human evolution.Nat. Rev. Genet. 2012; 13: 745-753Crossref PubMed Scopus (343) Google Scholar, 2Groucutt H.S. Petraglia M.D. Bailey G. Scerri E.M. Parton A. Clark-Balzan L. Jennings R.P. Lewis L. Blinkhorn J. Drake N.A. et al.Rethinking the dispersal of Homo sapiens out of Africa.Evol. Anthropol. 2015; 24: 149-164Crossref PubMed Scopus (210) Google Scholar]. Two categories of models are proposed for the dispersal of non-Africans: (1) single dispersal, i.e., a single major diffusion of modern humans across Eurasia and Australasia [3Mellars P. Gori K.C. Carr M. Soares P.A. Richards M.B. Genetic and archaeological perspectives on the initial modern human colonization of southern Asia.Proc. Natl. Acad. Sci. USA. 2013; 110: 10699-10704Crossref PubMed Scopus (217) Google Scholar, 4Macaulay V. Hill C. Achilli A. Rengo C. Clarke D. Meehan W. Blackburn J. Semino O. Scozzari R. Cruciani F. et al.Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes.Science. 2005; 308: 1034-1036Crossref PubMed Scopus (566) Google Scholar, 5Oppenheimer S. A single southern exit of modern humans from Africa: before or after Toba?.Quat. Int. 2012; 258: 88-99Crossref Scopus (56) Google Scholar]; and (2) multiple dispersal, i.e., additional earlier population expansions that may have contributed to the genetic diversity of some present-day humans outside of Africa [6Lahr M.M. Foley R.A. Towards a theory of modern human origins: geography, demography, and diversity in recent human evolution.Am. J. Phys. Anthropol. 1998; : 137-176Crossref PubMed Google Scholar, 7Maca-Meyer N. González A.M. Larruga J.M. Flores C. Cabrera V.M. Major genomic mitochondrial lineages delineate early human expansions.BMC Genet. 2001; 2: 13Crossref PubMed Scopus (265) Google Scholar, 8Reyes-Centeno H. Ghirotto S. Détroit F. Grimaud-Hervé D. Barbujani G. Harvati K. Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia.Proc. Natl. Acad. Sci. USA. 2014; 111: 7248-7253Crossref PubMed Scopus (114) Google Scholar, 9Armitage S.J. Jasim S.A. Marks A.E. Parker A.G. Usik V.I. Uerpmann H.P. The southern route "out of Africa": evidence for an early expansion of modern humans into Arabia.Science. 2011; 331: 453-456Crossref PubMed Scopus (385) Google Scholar]. Many variants of these models focus largely on Asia and Australasia, neglecting human dispersal into Europe, thus explaining only a subset of the entire colonization process outside of Africa [3Mellars P. Gori K.C. Carr M. Soares P.A. Richards M.B. Genetic and archaeological perspectives on the initial modern human colonization of southern Asia.Proc. Natl. Acad. Sci. USA. 2013; 110: 10699-10704Crossref PubMed Scopus (217) Google Scholar, 4Macaulay V. Hill C. Achilli A. Rengo C. Clarke D. Meehan W. Blackburn J. Semino O. Scozzari R. Cruciani F. et al.Single, rapid coastal settlement of Asia revealed by analysis of complete mitochondrial genomes.Science. 2005; 308: 1034-1036Crossref PubMed Scopus (566) Google Scholar, 5Oppenheimer S. A single southern exit of modern humans from Africa: before or after Toba?.Quat. Int. 2012; 258: 88-99Crossref Scopus (56) Google Scholar, 8Reyes-Centeno H. Ghirotto S. Détroit F. Grimaud-Hervé D. Barbujani G. Harvati K. Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia.Proc. Natl. Acad. Sci. USA. 2014; 111: 7248-7253Crossref PubMed Scopus (114) Google Scholar, 9Armitage S.J. Jasim S.A. Marks A.E. Parker A.G. Usik V.I. Uerpmann H.P. The southern route "out of Africa": evidence for an early expansion of modern humans into Arabia.Science. 2011; 331: 453-456Crossref PubMed Scopus (385) Google Scholar]. The genetic diversity of the first modern humans who spread into Europe during the Late Pleistocene and the impact of subsequent climatic events on their demography are largely unknown. Here we analyze 55 complete human mitochondrial genomes (mtDNAs) of hunter-gatherers spanning ∼35,000 years of European prehistory. We unexpectedly find mtDNA lineage M in individuals prior to the Last Glacial Maximum (LGM). This lineage is absent in contemporary Europeans, although it is found at high frequency in modern Asians, Australasians, and Native Americans. Dating the most recent common ancestor of each of the modern non-African mtDNA clades reveals their single, late, and rapid dispersal less than 55,000 years ago. Demographic modeling not only indicates an LGM genetic bottleneck, but also provides surprising evidence of a major population turnover in Europe around 14,500 years ago during the Late Glacial, a period of climatic instability at the end of the Pleistocene.