The Arabian Cradle: Mitochondrial Relicts of the First Steps along the Southern Route out of Africa
2012; Elsevier BV; Volume: 90; Issue: 2 Linguagem: Inglês
10.1016/j.ajhg.2011.12.010
ISSN1537-6605
AutoresVerónica Fernandes, Farida Alshamali, Marco G. Alves, Marta D. Costa, Joana B. Pereira, Nuno Silva, Lotfi Cherni, Nourdin Harich, Viktor Černý, Pedro Soares, Martin Richards, Luı́sa Pereira,
Tópico(s)Pleistocene-Era Hominins and Archaeology
ResumoA major unanswered question regarding the dispersal of modern humans around the world concerns the geographical site of the first human steps outside of Africa. The "southern coastal route" model predicts that the early stages of the dispersal took place when people crossed the Red Sea to southern Arabia, but genetic evidence has hitherto been tenuous. We have addressed this question by analyzing the three minor west-Eurasian haplogroups, N1, N2, and X. These lineages branch directly from the first non-African founder node, the root of haplogroup N, and coalesce to the time of the first successful movement of modern humans out of Africa, ∼60 thousand years (ka) ago. We sequenced complete mtDNA genomes from 85 Southwest Asian samples carrying these haplogroups and compared them with a database of 300 European examples. The results show that these minor haplogroups have a relict distribution that suggests an ancient ancestry within the Arabian Peninsula, and they most likely spread from the Gulf Oasis region toward the Near East and Europe during the pluvial period 55–24 ka ago. This pattern suggests that Arabia was indeed the first staging post in the spread of modern humans around the world. A major unanswered question regarding the dispersal of modern humans around the world concerns the geographical site of the first human steps outside of Africa. The "southern coastal route" model predicts that the early stages of the dispersal took place when people crossed the Red Sea to southern Arabia, but genetic evidence has hitherto been tenuous. We have addressed this question by analyzing the three minor west-Eurasian haplogroups, N1, N2, and X. These lineages branch directly from the first non-African founder node, the root of haplogroup N, and coalesce to the time of the first successful movement of modern humans out of Africa, ∼60 thousand years (ka) ago. We sequenced complete mtDNA genomes from 85 Southwest Asian samples carrying these haplogroups and compared them with a database of 300 European examples. The results show that these minor haplogroups have a relict distribution that suggests an ancient ancestry within the Arabian Peninsula, and they most likely spread from the Gulf Oasis region toward the Near East and Europe during the pluvial period 55–24 ka ago. This pattern suggests that Arabia was indeed the first staging post in the spread of modern humans around the world. The genetic and archaeological focus on the Arabian Peninsula in the last few years has been motivated by the hypothesis that this region was probably the initial staging post in the first successful migration of anatomically modern humans out of Africa.1Macaulay 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, 2Thangaraj K. Chaubey G. Kivisild T. Reddy A.G. Singh V.K. Rasalkar A.A. Singh L. Reconstructing the origin of Andaman Islanders.Science. 2005; 308: 996Crossref PubMed Scopus (236) Google Scholar, 3Oppenheimer S. Out of Eden: The peopling of the World. Robinson Publishing, London2003Google Scholar mtDNA data suggest that people bearing haplogroup L3 migrated from the Horn of Africa4Torroni A. Achilli A. Macaulay V. Richards M. Bandelt H.-J. Harvesting the fruit of the human mtDNA tree.Trends Genet. 2006; 22: 339-345Abstract Full Text Full Text PDF PubMed Scopus (353) Google Scholar, 5Richards M. Bandelt H.J. Kivisild T. Oppenheimer S. A model for the dispersal of modern humans out of Africa.in: Bandelt H.-J. Macaulay V. Richards M. Mitochondrial DNA and the evolution of Homo sapiens. Springer-Verlag, Berlin2006: 225-265Google Scholar and recent evidence from complete sequences and improved molecular-dating techniques point to the origin of L3 within Africa ∼60–70 thousand years (ka) ago.6Soares P. Alshamali F. Pereira J.B. Fernandes V. Silva N.M. Afonso C. Costa M.D. Musilova E. Macaulay V. Richards M.B. et al.The expansion of mtDNA haplogroup L3 within and out of Africa.Mol. Biol. Evol. 2012; (Published online November 16, 2011)https://doi.org/10.1093/molbev/msr245Crossref PubMed Scopus (182) Google Scholar A key question is where L3 evolved into the two non-African haplogroups N and M. Together, N and M encompass all of the deeply rooted variation observed in the rest of the world.4Torroni A. Achilli A. Macaulay V. Richards M. Bandelt H.-J. Harvesting the fruit of the human mtDNA tree.Trends Genet. 2006; 22: 339-345Abstract Full Text Full Text PDF PubMed Scopus (353) Google Scholar Haplogroup N and its major subclade, haplogroup R, are ubiquitous in non-Africans and thus must have evolved very early in the dispersal process. Haplogroup M, on the other hand, is found primarily in the Indian subcontinent and farther east and has a single subclade, M1, that spread back into the Mediterranean region and eastern Africa during the Late Pleistocene.7Olivieri A. Achilli A. Pala M. Battaglia V. Fornarino S. Al-Zahery N. Scozzari R. Cruciani F. Behar D.M. Dugoujon J.-M. et al.The mtDNA legacy of the Levantine early Upper Palaeolithic in Africa.Science. 2006; 314: 1767-1770Crossref PubMed Scopus (197) Google Scholar The age of the haplogroup N founder in western Eurasians has been estimated at ∼50–65 ka,8Soares P. Ermini L. Thomson N. Mormina M. Rito T. Röhl A. Salas A. Oppenheimer S. Macaulay V. Richards M.B. Correcting for purifying selection: An improved human mitochondrial molecular clock.Am. J. Hum. Genet. 2009; 84: 740-759Abstract Full Text Full Text PDF PubMed Scopus (537) Google Scholar very close to the age of their ancestral L3 clade in Africa, suggesting that a single, continuous demographic process might explain both the initial diversification and expansion of L3 in eastern Africa and the exit of modern humans from Africa.6Soares P. Alshamali F. Pereira J.B. Fernandes V. Silva N.M. Afonso C. Costa M.D. Musilova E. Macaulay V. Richards M.B. et al.The expansion of mtDNA haplogroup L3 within and out of Africa.Mol. Biol. Evol. 2012; (Published online November 16, 2011)https://doi.org/10.1093/molbev/msr245Crossref PubMed Scopus (182) Google Scholar This process is likely to have been linked to the improved climatic conditions after ∼70 ka ago in eastern Africa and contradicts the recent suggestion of population continuity in eastern Arabia ∼120 ka ago.9Rose J.I. New light on human prehistory in the Arabo-Persian Gulf Oasis.Curr. Anthropol. 2010; 51: 849-883Crossref Scopus (92) Google Scholar, 10Armitage 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 Strictly speaking, haplogroups N and R could have arisen anywhere in the region between Southwest Asia and Australasia; basal branches are found in this region today.1Macaulay V. Hill C. Achilli A. Rengo C. Clarke D. Meehan W. Blackburn J. Semino O. Scozzari R. 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Springer-Verlag, Berlin2006: 225-265Google Scholar Modern humans arrived in the Near East only ∼45–50 ka ago,11Shea J.J. Transitions or turnovers? Climatically-forced extinctions of Homo sapiens and Neandertals in the East Mediterranean Levant.Quat. Sci. Rev. 2008; 27: 2253-2270Crossref Scopus (146) Google Scholar most likely as a result of the desert barrier until climatic improvement ∼50 ka ago.1Macaulay 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, 3Oppenheimer S. Out of Eden: The peopling of the World. Robinson Publishing, London2003Google Scholar, 7Olivieri A. Achilli A. Pala M. Battaglia V. Fornarino S. Al-Zahery N. Scozzari R. Cruciani F. Behar D.M. 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Mitochondrial haplogroup N1a phylogeography, with implication to the origin of European farmers.BMC Evol. Biol. 2010; 10: 304PubMed Google Scholar Haplogroup N1b is also very rare, but one subclade, N1b2, is quite common in Jews, and a Near Eastern origin and founder effect in Ashkenazi ancestors has been suggested.19Kivisild T. Reidla M. Metspalu E. Rosa A. Brehm A. Pennarun E. Parik J. Geberhiwot T. Usanga E. Villems R. Ethiopian mitochondrial DNA heritage: Tracking gene flow across and around the gate of tears.Am. J. Hum. Genet. 2004; 75: 752-770Abstract Full Text Full Text PDF PubMed Scopus (202) Google Scholar, 20Behar D.M. Metspalu E. Kivisild T. Achilli A. Hadid Y. Tzur S. Pereira L. Amorim A. Quintana-Murci L. Majamaa K. et al.The matrilineal ancestry of Ashkenazi Jewry: Portrait of a recent founder event.Am. J. Hum. Genet. 2006; 78: 487-497Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar, 21Behar D.M. Metspalu E. Kivisild T. Rosset S. Tzur S. Hadid Y. 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The Druze: A population genetic refugium of the Near East.PLoS ONE. 2008; 3: e2105Crossref PubMed Scopus (35) Google Scholar We analyzed a total of 2,362 N(xR) HVS-I sequences from the literature from a total of 32,812 individuals surveyed (Table S2) and classified them with the aid of PhyloTree.33van Oven M. Kayser M. Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation.Hum. Mutat. 2009; 30: E386-E394Crossref PubMed Scopus (1336) Google Scholar For the phylogeny reconstruction, preliminary reduced-median network analyses34Bandelt H.-J. Forster P. Sykes B.C. Richards M.B. Mitochondrial portraits of human populations using median networks.Genetics. 1995; 141: 743-753PubMed Google Scholar led to a suggested branching order for the trees, which we then constructed most parsimoniously by hand. For estimation of the time to most recent common ancestor (TMRCA) for specific clades in the phylogeny, we used the ρ statistic35Forster P. Harding R. Torroni A. Bandelt H.-J. Origin and evolution of Native American mtDNA variation: A reappraisal.Am. J. Hum. Genet. 1996; 59: 935-945PubMed Google Scholar and maximum likelihood (ML) as described previously.8Soares P. Ermini L. Thomson N. Mormina M. Rito T. Röhl A. Salas A. Oppenheimer S. Macaulay V. Richards M.B. Correcting for purifying selection: An improved human mitochondrial molecular clock.Am. J. Hum. Genet. 2009; 84: 740-759Abstract Full Text Full Text PDF PubMed Scopus (537) Google Scholar In order to detect population growth associated with the N(xR) lineages, we obtained Bayesian skyline plots (BSPs)36Drummond A.J. Rambaut A. Shapiro B. Pybus O.G. Bayesian coalescent inference of past population dynamics from molecular sequences.Mol. Biol. Evol. 2005; 22: 1185-1192Crossref PubMed Scopus (2291) Google Scholar, 37Atkinson Q.D. Gray R.D. Drummond A.J. Bayesian coalescent inference of major human mitochondrial DNA haplogroup expansions in Africa.Proc. Biol. 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Population expansion in the North African late Pleistocene signalled by mitochondrial DNA haplogroup U6.BMC Evol. Biol. 2010; 10: 390Crossref PubMed Scopus (48) Google Scholar We generated BSPs for each of the main subclades and subregions and visualized the plots with Tracer v1.3. We had two goals in performing these two subsets of analyses. First, we aimed to distinguish which haplogroups were mainly responsible for the increases in effective population sizes observed in the overall N(xR) analysis. Second, we aimed to observe whether a given region contained the signal for a given population increase in its specific N(xR) sequences. Such a signal would indicate a possible expansion involving several subclades within that region. To visualize the geographical distribution of N(xR) and its subclades, we constructed interpolation maps of HVS-I data by using the "Spatial Analyst Extension" of ArcView version 3.2 as described before.6Soares P. Alshamali F. Pereira J.B. Fernandes V. Silva N.M. Afonso C. Costa M.D. Musilova E. Macaulay V. Richards M.B. et al.The expansion of mtDNA haplogroup L3 within and out of Africa.Mol. Biol. Evol. 2012; (Published online November 16, 2011)https://doi.org/10.1093/molbev/msr245Crossref PubMed Scopus (182) Google Scholar, 39Pereira L. Silva N.M. Franco-Duarte R. Fernandes V. Pereira J.B. Costa M.D. Martins H. Soares P. Behar D.M. Richards M.B. Macaulay V. Population expansion in the North African late Pleistocene signalled by mitochondrial DNA haplogroup U6.BMC Evol. Biol. 2010; 10: 390Crossref PubMed Scopus (48) Google Scholar We reconstructed, haplogroup by haplogroup, HVS-I networks between nucleotide positions 16,051 and 16,400.32Andrews R.M. Kubacka I. Chinnery P.F. Lightowlers R.N. Turnbull D.M. Howell N. Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA.Nat. Genet. 1999; 23: 147Crossref PubMed Scopus (2551) Google Scholar In order to detect migrations from Southwest Asia to Europe and northern Africa, we employed a founder analysis for the N(xR) sequences and two criteria (f1 and f2) for identifying founder sequences.6Soares P. Alshamali F. Pereira J.B. Fernandes V. Silva N.M. Afonso C. Costa M.D. Musilova E. Macaulay V. Richards M.B. et al.The expansion of mtDNA haplogroup L3 within and out of Africa.Mol. Biol. Evol. 2012; (Published online November 16, 2011)https://doi.org/10.1093/molbev/msr245Crossref PubMed Scopus (182) Google Scholar, 16Richards M. Macaulay V. Hickey E. Vega E. Sykes B. Guida V. Rengo C. Sellitto D. Cruciani F. Kivisild T. et al.Tracing European founder lineages in the Near Eastern mtDNA pool.Am. J. Hum. Genet. 2000; 67: 1251-1276Abstract Full Text Full Text PDF PubMed Scopus (781) Google Scholar We scanned the distribution of founder ages for each region and defined equally spaced 200 yr intervals for each migration from 0–100 ka ago. Figure 1 presents an outline topology of the three basal west-Eurasian haplogroups within N(xR) and indicates the primary branches with ages scaled against the ML estimates. The lineages coalesce at ∼60 ka ago, a plausible estimate for the early stages of the out-of-Africa migration in western Eurasia, considering that at least 50 ka ago, modern humans were already present in Southeast Asia.40Barker G. Barton H. Bird M. Daly P. Datan I. Dykes A. Farr L. Gilbertson D. Harrisson B. Hunt C. et al.The 'human revolution' in lowland tropical Southeast Asia: The antiquity and behavior of anatomically modern humans at Niah Cave (Sarawak, Borneo).J. Hum. Evol. 2007; 52: 243-261Crossref PubMed Scopus (342) Google Scholar The complete phylogeny is shown in Tree S1 and includes age estimates obtained from complete genome (ρ and ML) and synonymous (ρ) clocks. Before focusing in detail on the history of the three haplogroups, we summarize here the overall pattern. Assuming a Near Eastern source and migrations into Europe and using an extensive HVS-I database, we obtained the following results (Figure S1): (1) a poorly defined peak ∼12 ka ago with the f1 criterion and (2) two other peaks, a small one dating to ∼6 ka ago and a larger one dating to ∼15 ka ago, with the f2 criterion. These results suggest that the three clades are primarily related to Late Glacial or postglacial expansions into Europe. We also performed a similar founder analysis of the three clades from the Near East into northern Africa, and we obtained a single peak, dating to 10.4 ka ago with the f1 criterion and to 13.8 ka ago with the f2 criterion. These peaks also indicate a primarily postglacial or Late Glacial expansion into this region. The BSP obtained from the overall data (Figure S2A) shows a continuous, slightly stepped increase from ∼15 ka ago almost to the present (Table 1). The BSP with only the European data (Figure S2B) separates two steps (∼13 ka and ∼6 ka ago), whereas the BSP for the pool of the Near East and Arabian Peninsula (Figure S2C) indicates only a period of increase, which was initially gradual, from ∼15 ka ago.Table 1Peaks of Rate of Population-Size Change through Time as Obtained from the BSPsDataPeak (ka)Range (ka)IncrementaIncrement rate corresponds to the number of times the effective population size increased during this period.RegionOverall5.6; 12.631.78–14.6742.49Near East, Caucasus, Arabian Peninsula9.347.70–14.2116.85Europe2.940.78–5.295.3212.8011.18–14.722.71HaplogroupN13.601.51–6.0620.0511.2911.77–13.373.80N26.293.15–10.1119.99N2 (without haplogroup W in Finns)7.814.59–11.223.70X6.364.49–8.305.7113.7211.73–16.163.46The rate of population-size increase was of at least one individual per 100 individuals in a period of 100 yr.a Increment rate corresponds to the number of times the effective population size increased during this period. Open table in a new tab The rate of population-size increase was of at least one individual per 100 individuals in a period of 100 yr. Haplogroup N1, at ∼50–63 ka of age, is the oldest N(xR) clade, and it probably originated in Southwest Asia and split early into two branches. The first branch, N1a′c′d′e′I, comprises a series of subclades (N1a, N1c, N1d, N1e, and I) dating to 46–57 ka ago and was found across Southwest Asia (including the Near East and Arabia) and Europe, but many of the most basal lineages within the subclades were restricted to Southwest Asia. Within N1′a′c′d′e′I, there is a series of consecutive splits. N1c represents the earliest, at ∼47 ka old, and it is seen primarily in Southwest Asia, especially in Arabia (Figure 2D ). It is followed by N1d (the sample does not allow dating), detected so far only in India. Then, N1a separated from N1e′I ∼42 ka ago. N1a dates to ∼20 ka ago and, like N1c, is most frequent in Arabia (Figure 2B). Strikingly, there are several deeply rooted Ethiopian, Somali, and Yemeni lineages within N1a. The position in the tree of the mutation at position 152 within N1a is ambiguous; potentially, this subclade could split before the main N1a clade, but it is more likely (given the diversity of the subclade, dating to ∼15 ka ago, compared to the age of N1a of ∼20 ka) that it split within N1a and can be referred to as N1a2. Either way, the N1a samples display deep diversity within eastern Africa and the southern part of the Arabian Peninsula, two places where the clade is most frequent,
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