Single, Rapid Coastal Settlement of Asia Revealed by Analysis of Complete Mitochondrial Genomes

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Science  13 May 2005:
Vol. 308, Issue 5724, pp. 1034-1036
DOI: 10.1126/science.1109792


A recent dispersal of modern humans out of Africa is now widely accepted, but the routes taken across Eurasia are still disputed. We show that mitochondrial DNA variation in isolated “relict” populations in southeast Asia supports the view that there was only a single dispersal from Africa, most likely via a southern coastal route, through India and onward into southeast Asia and Australasia. There was an early offshoot, leading ultimately to the settlement of the Near East and Europe, but the main dispersal from India to Australia ∼65,000 years ago was rapid, most likely taking only a few thousand years.

The traditional “out of Africa” model for modern human origins posits an ancestry in sub-Saharan Africa, followed by a dispersal via the Levant ∼45,000 years ago (1, 2). However, the suggestion of an earlier “southern route” dispersal from the Horn of Africa ∼60,000 to 75,000 years ago, along the tropical coast of the Indian Ocean to southeast Asia and Australasia (3, 4), has recently gained ground (5-8). Part of its rationale has been the presence of a number of “relict” populations in southern India and southeast Asia; it has been suggested that these populations might be the descendants of such an earlier dispersal, along with Papuans and Aboriginal Australians (9).

Following the work of Vigilant et al. (10), Watson et al. (11) provided evidence from mitochondrial DNA (mtDNA) patterns for a single dispersal from Africa, although not distinguishing between a northern or southern route. More recently, the existence of a southern route has been supported by analyses of mtDNA restriction enzyme data from New Guinea (12) and control region sequences from mainland India and the Andaman Islands (13-16). Meanwhile, archaeological evidence has been found for the occupation of the coast of Eritrea ∼125,000 years ago—the oldest known indication of human exploitation of marine resources (17).

However, the published genetic data remain sufficiently ambiguous for some geneticists to reject the very existence of a southern route (18), and the question of single versus multiple dispersals also remains in dispute. What is needed to distinguish between the different dispersal hypotheses are well-resolved sequence data from the relict populations themselves. Here, we test the possible dispersal routes with a maximum likelihood analysis of complete mtDNA genomes from the Orang Asli—the aboriginal inhabitants of Malaysia and the principal relict group in southeast Asia (19)—in the context of other eastern Eurasian and Australasian lineages.

We sampled 260 maternally unrelated Orang Asli, including (i) Semang, who live (or lived until recently) in small, nomadic hunter-gatherer groups in the lowland rainforests; (ii) Senoi, who are traditionally swidden agriculturalists; and (iii) Aboriginal Malays, horticulturalists and fishers who most resemble physically the majority Melayu Malays. It is widely agreed that the Orang Asli, especially the Semang, are aboriginal inhabitants of the Malay Peninsula (19, 20). Moreover, there is a well-documented archaeological record of continuous occupation by hunter-gatherers throughout the Holocene, and an essentially continuous hunter-gatherer record from at least 40,000 (perhaps 70,000) years ago (21).

A reconstructed phylogeny of eastern Eurasian mtDNA genomes is shown in Fig. 1 (see fig. S1 for branch labels); ages of the principal nodes in the tree are shown in table S3. This analysis yields a time to the most recent common ancestor of all humans (TMRCA) of ∼200,000 years ago, in close agreement with Mishmar et al. (22). Haplogroup L3 (the African clade that gave rise to the two basal non-African clades, haplogroups M and N) is ∼84,000 years old, and haplogroups M and N themselves are almost identical in age at ∼63,000 years old, with haplogroup R diverging rapidly within haplogroup N ∼60,000 years ago. This agrees quite well with the similarity of ages of M and N noted by Forster et al. (12) [see also (23)] and with the ages of both autochthonous R lineages in India (24) and the three major haplogroups in China (25).

Fig. 1.

Reconstructed phylogeny of 31 mtDNA coding region sequences. mtDNAs from the Malay Peninsula are indicated by solid circles at the tips of the tree.

Three possible hypotheses can be distinguished using these data. If modern non-Africans are descendants of populations that dispersed along both northern and southern routes, then mtDNA lineages belonging to relict populations (including Orang Asli, Papuans, and Aboriginal Australians) should diverge from founder types that are distinct from those leading to the main continental Eurasian groups. If there were just a single dispersal, then all non-African populations should diverge from the same set of founders, which would coalesce to ∼45,000 to 50,000 years ago if the Levantine corridor model were correct, or ∼60,000 to 75,000 years ago if they were all the result of the proposed earlier single southern route (4). At this time, a northern passage was most likely blocked by desert and semi-desert (26).

We assessed the distribution of mtDNAs present in the Orang Asli (table S2) by searching for their associated control region motifs in the worldwide mtDNA database (27). Several are shared with other southeast Asian populations, and these most likely indicate Holocene introgression (25, 28). However, most are virtually unique to the Orang Asli and are therefore likely to be indigenous. This strongly supports the suggestion that the Orang Asli harbor “relict” mtDNA lineages with time depths of ∼44,000 to 63,000 years (27). Their restricted distribution makes it very likely that these lineages diverged around that time within mainland southeast Asia. Although caution is warranted given the time depths involved, this conclusion is plausible on environmental grounds. Forests would have flourished on the lowlands abutting the Malaysian Peninsula throughout the last glacial period (21), which implies that this region acted as a glacial refuge where populations survived and genetic diversity was maintained. Although it is likely that waves of replacement occurred during the late Holocene to the north of the peninsula and on the coasts, it appears that they did not take place in the interior rainforest—or at least that the ancestors of the Orang Asli survived, albeit in low numbers, in Malaysia (20).

Furthermore, examination of recently published complete mtDNA genomes from Papuans and Aboriginal Australians (29) shows an analogous situation in which the lineages are predominantly unique to Australasia but diverge from the base of all three founder haplogroups. Both the indigenous Malaysian mtDNAs and those of Australasia are derived from the three major Eurasian founder haplogroups, M, N, and R, which are also found alongside one another to the west in the Indian subcontinent (15) as well as throughout continental Asia (25, 28).

The very similar ages of haplogroups M, N, and R indicate that they were part of the same colonization process [see (23)]. This most likely involved the exodus of a founding group of several hundred individuals (27) from East Africa, some time after the appearance of haplogroup L3 ∼85,000 years ago, followed by a period of mutation and drift during which haplogroups M, N, and R evolved and the ancestral L3 was lost. Although the details of this period remain to be elucidated, the next stage is much clearer. The presence in each region of the same three founder haplogroups, but differentiated into distinct subhaplogroups, indicates that there was a rapid coastal dispersal from ∼65,000 years ago around the Indian Ocean littoral and on to Australasia. Firm minimum archaeological age estimates are somewhat more recent— ∼50,000 years for Australia (30) and ∼45,000 years for southeast Asia (31)—but early evidence may have been lost to sea level rises. Moreover, human populations may then have diffused from the coast into the continental interiors more gradually, leaving a greater archaeological signature on the landscape as they grew in size.

This evidence suggests that this coastal trail was likely the only route taken during the Pleistocene settlement of Eurasia by the ancestors of modern humans, and that the primary dispersal process, at least from India to Australasia, was very rapid. A founder analysis of western, southern, and eastern Eurasian and Australasian complete mtDNAs suggested a shallow gradient of arrival times, from ∼66,000 years ago in India to ∼63,000 years ago in Australasia (table S4). Assuming a distance of ∼12,000 km, this allowed us to estimate a dispersal rate of ∼4 km/year from point estimates, a little lower than estimates for the more recent expansion into the Americas (32). An approximate lower bound on the dispersal rate is ∼0.7 km/year, comparable to the recolonization of Europe after the ice age (33).

By contrast with South Asians, eastern Eurasians, and Australasians, western Eurasians have a high level of haplogroup-level diversity within haplogroups N and R, but lack haplogroup M almost entirely (34). The colonization of western Eurasia has usually been thought to have been the result of a “northern route” dispersal out of Africa, through North Africa and the Levant (4), but the close similarity of the mtDNA founder age to that of India (table S4) suggests that it was most likely the result of an early offshoot of colonization along the southern route, followed by a lengthy pause until the climate improved (26) and the ancestors of western Eurasians were able to enter the Levant and Europe. This implies that the subsequent Upper Paleolithic “revolution” in western Eurasia was one regional indication of the emergence of modern humans, rather than a radical break with the past (35).

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Materials and Methods

Fig. S1

Tables S1 to S4


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