Population history of the Red SeaЧgenetic exchanges between the Arabian Peninsula and East Africa signaled in the mitochondrial DNA HV1 haplogroup.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:592–598 (2011) Population History of the Red Sea—Genetic Exchanges Between the Arabian Peninsula and East Africa Signaled in the Mitochondrial DNA HV1 Haplogroup Eliška Musilová,1 Verónica Fernandes,2,3 Nuno M. Silva,2 Pedro Soares,2 Farida Alshamali,4 Nourdin Harich,5 Lotﬁ Cherni,6,7 Amel Ben Ammar El Gaaied,6 Ali Al-Meeri,8 Luı́sa Pereira,2,9 and Viktor Černý10* 1 Department of Anthropology and Human Genetics, Faculty of Science, Charles University, Prague, Czech Republic Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), Porto, Portugal 3 Institute of Integrative and Comparative Biology, Faculty of Biological Sciences, University of Leeds, UK 4 Dubai Police GHQ, General Department of Forensic Sciences & Criminology, Dubai, United Arab Emirates 5 Laboratoire d’Anthropogénétique, Départment de Biologie, Université Chouaı̈b Doukkali, El Jadida, Morocco 6 Faculty of Sciences of Tunis, Laboratory of Genetics Immunology and Human Pathology, Tunis, Tunisia 7 Higher Institute of Biotechnology of Monastir, Tunisia 8 Department of Clinical Biochemistry, Faculty of Medicine and Health Sciences, University of Sana’a, Sana’a, Yemen 9 Faculdade de Medicina da Universidade do Porto, Portugal 10 Archaeogenetics Laboratory, Institute of Archaeology, Prague, Academy of Sciences of the Czech Republic, Czech Republic 2 KEY WORDS mtDNA genomes; HV1 haplogroup; Arabian Peninsula; East Africa ABSTRACT Archaeological studies have revealed cultural connections between the two sides of the Red Sea dating to prehistory. The issue has still not been properly addressed, however, by archaeogenetics. We focus our attention here on the mitochondrial haplogroup HV1 that is present in both the Arabian Peninsula and East Africa. The internal variation of 38 complete mitochondrial DNA sequences (20 of them presented here for the ﬁrst time) afﬁliated into this haplogroup testify to its emergence during the late glacial maximum, most probably in the Near East, with subsequent dispersion via population expansions when climatic conditions improved. Detailed phylogeography of HV1 sequences shows that more recent demographic upheavals likely contributed to their spread from West Arabia to East Africa, a ﬁnding concordant with archaeological records suggesting intensive maritime trade in the Red Sea from the sixth millennium BC onwards. Closer genetic exchanges are apparent between the Horn of Africa and Yemen, while Egyptian HV1 haplotypes seem to be more similar to the Near Eastern ones. Am J Phys Anthropol 145:592–598, 2011. V 2011 Wiley-Liss, Inc. The recent advances in sequencing technology enable us to get a much better picture of human population history than before. This is being achieved in part through the highly resolved phylogenetic inferences based on complete mitochondrial DNA (mtDNA) genomes. In fact, the association of these detailed phylogenies with a molecular clock allows us to focus on a speciﬁc time-frame of human evolution occurring in a particular geographic context and to disentangle information for diverse migrations which followed the same pathways. One important geographic route that has become a focus of interest in recent years is the one linking East Africa with the Arabian Peninsula through the Bab elMandeb strait. Some genetic studies inferred that this route has played a main role not only in the ﬁrst successful out-of-Africa migration of modern humans some 50–70 thousand years ago (KYA) (Macaulay et al., 2005; Thangaraj et al., 2005) but also in more recent occurrences such as the back to Africa migrations from Arabia revealed in the analysis of the Yemeni maternal gene pool (Černý et al., 2011) and in human movements resulting from the Arab slave trade from the seventh century onwards, further contributing to the spread of L haplogroups into Arabia (Richards et al., 2003; Kivisild et al., 2004; Harich et al., 2010). Archaeology has demonstrated several important periods of common history between East Africa and the Arabian Peninsula. There are two archaeological sites in the C 2011 V WILEY-LISS, INC. C Additional Supporting Information may be found in the online version of this article. Grant sponsors: Ministry of Education of the Czech Republic, Grant number: KONTAKT ME 917; the Council of American Overseas Research Centers; the American Institute for Yemeni Studies; the Portuguese Fundação para a Ciência e a Tecnologia (project PTDC/ANT/66275/2006; post-doc grant - SFRH/BPD/64233/2009; PhD grant - SFRH/BD/61342/2009); IPATIMUP is an Associate Laboratory of the Portuguese Ministry of Science, Technology and Higher Education, and is partially supported by FCT; the Portuguese Foundation for Science and Technology. *Correspondence to: Viktor Černý, Archaeogenetics Laboratory, Institute of Archaeology, Academy of Sciences of the Czech Republic, Prague 11801, Czech Republic. E-mail: firstname.lastname@example.org Received 24 November 2010; accepted 7 February 2011 DOI 10.1002/ajpa.21522 Published online 9 June 2011 in Wiley Online Library (wileyonlinelibrary.com). GENETIC EXCHANGES ACROSS THE RED SEA Yemeni highlands attesting to an Early Holocene ‘‘PreNeolithic’’ settlement throughout the eastern Yemen Plateau and a single continuum from Pre-Neolithic to Neolithic, with features of the Pre-Neolithic industry displaying hints of similarities with East Africa rather than the Fertile Crescent (Fedele, 2009). Another study (McCorriston and Martin, 2009) focused on the Early Holocene pastoralists along the desert margins of southern Arabia and found evidence for cattle introduction from the Levant or possibly from northeastern Africa by the sixth millennium BC, if not earlier. Moreover, many important trade links connected the two Red Sea coasts, including the obsidian trade network between the Horn of Africa and Arabia, which arose as early as the seventh to fourth millennia BC and continued up to the ﬁrst millennium BC (Zarins, 1989). In the mid-ﬁrst millennium BC, a south Arabian commercial network was established under the control of the so-called caravan kingdoms, especially that of Saba (Breton, 1999). At this time, a group of Semitic-speaking peoples—immigrants from Southern Arabia—arrived to Eritrea and Ethiopia to expand their commercial activities (Munro-Hay, 1991). It has been suggested that these trading colonists, who maintained their contact with their country of origin for centuries, brought not only a sea-based trading network but also a Semitic cultural tradition into the Cushitic substrate (Newman, 1995). Archaeogenetics has started revealing the importance of the period encompassing the end of the Pleistocene and Early Holocene, when major population expansions occurred in South Arabia, leaving evidence in the form of the internal diversiﬁcation of mtDNA haplogroup R0a (Černý et al., 2011). Considering the paleoclimatic data (Rose and Petraglia, 2009), the post-late glacial maximum (LGM) expansion around 16 KYA seemed to be especially important within southeast parts of Yemen (such as Al Mahra and Hadramawt) known as the South Arabian refugium. This climatically favorable period, coinciding roughly with the Bölling-Allerød interstadial, was only interrupted with the onset of the Younger Dryas 13.5 KYA, but was re-established in the Early Holocene when monsoon precipitation increased again some 9 KYA. Present climatic conditions started to develop from about 5 KYA onward (Parker, 2009). An example of the later demographic expansion was the development of R0a1a1a and R0a2f1 lineages especially in Soqotra Island, between 6 and 3 KYA (Černý et al., 2011), chronologically matching the earliest evidence for seafaring activity in the area (Boivin et al., 2009). Naturally, some of the R0a branches emerging in the Arabian Peninsula spread to East Africa as well. Together with R0a, HV1 lineages attain a frequency of 15.7% in Yemen (Černý et al., 2008), 18.4% in Saudi Arabia (Abu-Amero et al., 2008), 4.9% in Sudan (unpublished), 11.2% in Ethiopia (Kivisild et al., 2004), and unpublished), and 9.5% in Somalia (unpublished). There is not much information about the HV1 haplogroup, which is deﬁned by a transversion (A to T) at position Abbreviations HVRI IDW KYA ML mtDNA PCR TMRCA hypervariable region I inverse distance weighted thousand years ago maximum likelihood mitochondrial DNA polymerase chain reaction time of the most recent common ancestor 593 8,014 and two substitutions at positions 15,218 and 16,067 (van Oven and Kayser, 2009), except that it appeared contemporaneously with its sister clade R0a, around 20 KYA in the Near East. In this work, we focus on HV1 lineages found in Arabia, Eastern, and Northern Africa, and perform complete sequencing of 20 HV1 haplotypes to add new information to what is known on the population history of both sides of the Red Sea. MATERIALS AND METHODS Complete mtDNA sequencing A total of 20 HV1 haplotypes were selected for complete mtDNA sequencing from available datasets of hypervariable region I (HVRI) sequences (Černý et al., 2008; Cherni et al., 2009; Harich et al., 2010; and articles under preparation), previously deﬁned as HV1 for displaying a transition at control region position 16,067; the sample represents 12 haplotypes from Yemen, one from Sudan, one from Ethiopia, three from Somalia, two from Tunisia, and one from Morocco. Whole genome sequencing was conducted under conditions already published (Maca-Meyer et al., 2001; Pereira et al., 2007). Polymerase chain reaction (PCR) products were puriﬁed and sequenced using the forward primers only. However, in cases of the poly-C stretch between positions 568–573 and 16,184–16,193, the reverse primers were used as well. Sequencing was performed on an ABI 3100 DNA Analyzer (Applied Biosystems, Foster City, CA). Chromatograms were evaluated by two independent observers with the help of SeqScape (Applied Biosystems) and BioEdit version 220.127.116.11 (Hall, 1999). In cases of ambiguous results, new PCR ampliﬁcation and sequencing reactions were performed. The complete mtDNA sequences are deposited in GenBank database with accession numbers JF260932–JF260951. Phylogenetic analyses A preliminary reduced-median network analysis (Bandelt et al., 1995) led to a suggested branching structure for the tree of complete sequences, which was then checked and constructed by hand. All variable positions were used except 16182C, 16183C, and 16519, as they are inconsistently reported in the literature and are too recurrent. We also used 18 previously published whole HV1 genome sequences [AY738942 and AY738943 (Achilli et al., 2004), EF556168, EF556182, and EF556190 (Behar et al., 2008), FJ460547 (Costa et al., 2009), EF660935 and EF660936 (Gasparre et al., 2007), EU935461 (Kujanová et al., 2009), FJ210914, EF421157, DQ856316, EF396958, FJ210876, HM575427, HM998901, HQ165756, and HQ326986 from Family Tree DNA. In calculating the q statistic (mean divergence from inferred ancestral haplotype) for the time of the most recent common ancestor (TMRCA) of speciﬁc clades in the phylogeny, the complete sequence mutation rate estimates used were one substitution in every 3,624 years corrected for purifying selection, and one substitution in every 7,884 years for synonymous substitution (Soares et al., 2009), by using the calculator provided in that article. Standard errors were calculated as in Saillard et al. (Saillard et al., 2000). We obtained maximum likelihood (ML) estimates of branch lengths using PAML 3.13 (Yang, 1997), assuming the HKY85 mutation model with c-distributed rates (approximated by a discrete distribution with 32 categories). We converted mutational American Journal of Physical Anthropology 594 E. MUSILOVÁ ET AL. Fig. 1. Interpolation map for HV1 haplogroup. distance in ML into time using the complete mitochondrial genome clock (Soares et al., 2009). We also constructed a reduced-median network, with a reducing threshold of two, for HVRI diversity of HV1 haplotypes described in the literature (references presented in Supporting Information 1). The fastest sites [16,093, 16,129, 16,189, 16,311, and 16,362 (Soares et al., 2009)] were down-weighted to 5 from an overall value of 10 for all the remaining sites. Age estimates using the q statistic were obtained using the mutation rate of 1 substitution every 16,667 years for the HVRI region between positions 16,051 and 16,400 (Soares et al., 2009). Interpolation map To determine and visualize the geographical distribution of HV1, an interpolation map was drawn using the ‘‘spatial analyst extension’’ of ArcView version 3.2 (www.esri.com/software/arcview). The ‘‘inverse distance weighted’’ (IDW) option with a power of two was used for the interpolation of the surface. IDW assumes that each input point has a local inﬂuence that decreases with distance. The geographic location used is the center of the distribution area from where individual samples of each population were collected. RESULTS The geographic distribution of HV1 frequencies was plotted across the Arabian Peninsula, East Africa, and neighboring regions (see Fig. 1). Very high frequencies of HV1 are found around the Near East (including northeast Africa as well), where this haplogroup probably originated (see also the geographic location of the ancestral American Journal of Physical Anthropology haplotype in Fig. 3). The highest HV1 frequency was detected in Somalia, where, however no ancestral haplotypes were found. The HV1 phylogeny drawn based on information from 38 complete mtDNA sequences (see Fig. 2) shows an early split, with two Yemeni sequences missing the substitution (a medium recurrent mutation) at position 15,218 (Pereira et al., 2009; Soares et al., 2009). Although we have considered, based on the geography, the possibility that 15,218 might have back-mutated, the argument is not really strong enough to lead us not to present a parsimonious reconstruction. In either case, these sequences represent an extra HV1 branch—HV1 proper is thus split into two main branches each deﬁned by a single coding region transition: a transition at position 8277 deﬁning HV1a, and position 12,696 enclosing HV1b lineages. Three other rarer lineages derive from the root of HV1. An extra main branch of HV1 could be considered if we assume that 15,218 reverted in the above-mentioned branch. Group HV1a is further split into three sub-haplogroups—the previously deﬁned HV1a1 (with transition at positions 150, 15,927, and 16,355), HV1a2 (transition at 4,596), and the newly designated HV1a3 (transition at 3,421 and transversion C to A at 16,327). The three Yemeni sequences described in this work belonging to sub-haplogroup HV1a1 present the common 9bp deletion (Cann and Wilson, 1983), sometimes deﬁned between positions 8,281–8,289 (Kong et al., 2006) but here more parsimoniously deﬁned between positions 8,272–8,280, since it is missing the haplogroup deﬁning position 8,277. The HV1b group has a main branch—sub-haplogroup HV1b1—bearing transitions at positions 2,626, 4,739, 7,598, and 16,274. The sub-haplogroup HV1b2 presents substitutions at positions 152, 3,547, 6,023, and 16,189. From the complete mtDNA tree (see Fig. 2), HV1a3 and HV1b1 seem to be restricted to Yemen and East Africa. It is noteworthy that although the ﬁrst branch split of the HV1 haplogroup does not show diversity in HVRI, most of its internal branches can be differentiated according to the variants in this region (except most of HV1a2). This allowed us to search in the HVRI datasets, which have a much larger number of samples, for sequences with substitution at positions 16,067 (HV1) and 16,355 (HV1a1) or 16,327A (HV1a3), 16,192 (a subbranch of HV1a2), 16,274 (HV1b1), 16,189 (HV1b2), 16,234 (a sub-branch of HV1b), 16,172 (HV1c), and 16,242 (a sub-branch of HV1). We must take into account that some of these are fast-evolving sites and that they could be deﬁning false monophyletic clades. A total of 187 HV1 sequences with known geographical origin were collected. The haplotypes are displayed in the network in Figure 3. In fact, sub-haplogroup HV1a3 has been observed only in Africa (in one Egyptian and one Ethiopian sample) and in Arabia (one Saudi and four Yemeni); sub-haplogroup HV1b1 was also mainly found in Africa (10 Somali, two Nubian, one Egyptian, and one Ethiopian) and Arabia (12 Yemeni Jewish, seven Yemeni, and one Bedouin), with a few instances in other places (one Caucasus and one Near Eastern). Sub-haplogroup HV1a1 is geographically widespread (ﬁve Caucasus, one Egyptian, one European, 43 Caucasus Jewish, four Near Eastern, and three Yemeni). Curiously, the HV1 root haplotype with substitution at position 16,067 was not observed in the Arabian Peninsula except in four Yemeni Jews, but was observed in 11 Caucasus, four Egyptian, one European, two Maghreb, and six Near Eastern GENETIC EXCHANGES ACROSS THE RED SEA 595 Fig. 2. Phylogeny of the complete HV1 mtDNA sequences. Integers represent transition, only when a sufﬁx ‘‘A,’’ ‘‘G,’’ ‘‘C,’’ or ‘‘T’’ is appended, then it indicates a transversion. Deletions are indicated by a ‘‘del’’ following the deleted nucleotide position. Integers in bold indicate synonymous substitutions. Dates indicated are based on diversity for the complete molecule, only synonymous polymorphisms (in bold) and ML estimates (underlined). ‘‘rCRS’’—revised Cambridge Reference Sequence; the insertion at 3151C was left out. samples, thus supporting a possible origin in the Near East. Haplotype 16,067–16,362, possibly deﬁning a preHV1 haplogroup, has so far been observed in Dubai (one), Ethiopia (four), Maghreb (one), and Yemen (three). The complete sequencing allowed the application of the mutation rate estimate with a correction for purifying selection, as well as a clock based only on synonymous mutations, both recently published (Soares et al., 2009). The TMRCA estimate for HV1 was 22,350 (14,737–30,227) years when taking into consideration the sequences without the polymorphism at 15,218—a ﬁgure which closely matches the estimate of 18,695 (13,094–24,449) years when not considering those two sequences. The control region age estimate of HV1 also presents a similar age, dating to 19,430 (6,840–32,023) years. Age estimates of HV1 daughter sub-haplogroups are only slightly lower—15,178 (8,893–21,671) years for HV1a and 17,682 (10,320–25,316) years for HV1b. The common Arabian Peninsula and East African sub-haplogroups HV1a3 and HV1b1 share a close age of 6,549 (2,456–10,746) years and 10,268 (4,792–15,918) years, respectively. Sub-haplogroups HV1a1 and HV1a2, American Journal of Physical Anthropology 596 E. MUSILOVÁ ET AL. Fig. 3. Network for HVRI diversity in several regional populations. which despite being rare seem to have a wider geographical distribution, have TMRCA of 10,268 (3,602–17,194) years and 9,518 (3,963–15,255) years, respectively. The ratio of the dates based on the q statistic for the synonymous clock relative to the complete sequence was 1.24, closely overlapping in most branches except for HV1a1 which has a very broad age estimate based only on synonymous diversity [23,616 (4,917–42,315) years]. When testing ML estimates for the complete molecule, better concordance (0.96) was obtained with the ratio between ML and the q statistic. DISCUSSION The mtDNA gene pool of the West Arabian Peninsula displays signs of population expansions in lineages which have most probably been introduced here from the Near East. This is the pattern observed for HV1, which, together with R0a, constitute a considerable proportion of R and even N haplogroups observed in this geographic region [respectively, 63% and 22% in Saudi Arabia (Abu-Amero et al., 2008); and 76% and 25% in Yemen (Černý et al., 2008)]. HV1 presents an age overlapping the LGM period [22,350 (14,737–30,227) years], coincident with the age obtained for R0a haplogroup [22,588 (20,886–24,290) years; Černý et al., 2011]. Y chromosome diversity also reveals that the Arabian Peninsula mainly received its lineages from the Near East from the LGM onwards (Abu-Amero et al., 2009). It has been shown that Y chromosome population structure across the Peninsula was modulated by geography, along a west-east axis (Abu-Amero et al., 2009; Alshamali et al., 2009). Local population expansions in the post-LGM and early Holocene seem to have occurred in the Near East American Journal of Physical Anthropology (Roostalu et al., 2007) and the Arabian Peninsula (Černý et al., 2011). The HV1 tree also shows branching in starlike sub-haplogroups matching these periods, such as in HV1a [15,178 years (8,893–21,671)] and HV1b [17,682 years (10,320–25,316)]. These dates overlap the dates for the main R0a branches (Černý et al., 2011): 11,489 years (9,503–13,475) for R0a1a; 15,608 years (13,742–17,474) for R0a2; and 12,455 years (5,801–19,109) for R0a3. HV1 can be interpreted as a haplogroup whose geographic spread was facilitated by migration activity across the Red Sea as part of the post-LGM expansions occurring in the West of the Arabian Peninsula. Most probably some lineages of HV1 such as HV1a3 and HV1b1 passed from South Arabia to East Africa during the periods of intense commercial network activity that might have started, as is suggested by the archaeological evidence (Boivin et al., 2009), already in the sixth millennium BC. The fact that the East African lineages are not derivative of the Arabian ones, but diverge from the root of the sub-haplogroups, seems to indicate that the migration toward Africa happened soon after the emergence of the sub-haplogroups rather than recently. This pattern is similar to the one displayed by some R0a branches such as R0a2b [10,063 (5,467–14,659) years] and R0a2g [6,094 (1,558–10,630) years], published earlier (Černý et al., 2011). Intense maritime activity led not only to the expansion of lineages from the Arabian Peninsula to East Africa but also to the settlement of Soqotra Island in the Arabian Sea (Černý et al., 2009; Černý et al., 2011). Interestingly, the ﬂow of migrations from East Africa to the Arabian Peninsula seem to have been more recent, occurring mainly during the Arab-conducted slave trade initiated only in the seventh century AD (Richards et al., 2003; Kivisild et al., 2004). Curiously, Kivisild et al. (2004) detected a high proportion GENETIC EXCHANGES ACROSS THE RED SEA (12%) of the sub-Saharan L6 sequences in their Yemeni sample, suggesting that these sequences could be explained by an earlier gene ﬂow across the Red Sea; this observation was not reproduced, however, in other and larger Yemeni sample sets (Černý et al., 2008; Černý et al., 2009). It appears that Egypt received some N lineages directly from the Near East after the LGM, as is testiﬁed to by the higher match of Egyptian HV1 lineages with widespread haplotypes found in this study, as well as by genetic evidence collected earlier (Rowold et al., 2007). The close connection of HV1 between Egypt and the Near East, together with the geographical distribution of other haplogroups such as J, T, R0a, U6, H1, H3, or V show that North Africa can be genetically divided into an eastern and a western part. Although the ﬁrst was inﬂuenced by Near Eastern population expansions in the end of the Pleistocene and in the Holocene, the western part seems to show mainly post-LGM population expansions of the by-that-time autochthonous lineage U6 (Pereira et al., 2010a) and of European lineages such as H1, H3, and V that probably stemmed from the Iberian refugium (Cherni et al., 2009; Ennafaa et al., 2009; Pereira et al., 2010b). The question of how far the Near Eastern inﬂuence in North Africa extends remains. According to some genetic data, the imaginary line could be detected somewhere between Libya and Algeria (Dupanloup et al., 2000). Unfortunately, Libyan mtDNA sequences are still not currently available to address these issues. 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