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Major genomic mitochondrial lineages delineate early human expansions

Nicole Maca-Meyer, Ana M González, José M Larruga, Carlos Flores and Vicente M Cabrera*

BMC Genetics 2001, 2:13  doi:10.1186/1471-2156-2-13

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Mitochondrial footsteps of the Old World human colonization: A single origin, several dispersal hypothesis. José M. Larruga, Ana M. González, Nicole Maca-Meyer, Carlos Flores and Vicente M. Cabrera

Vicente Cabrera   (2004-10-29 15:59)  Department of Genetics, University of La Laguna email

The hypothesis that Homo s. sapiens originated in Africa and later colonized Eurasia replacing the descendents of H. erectus is now widely accepted. However, the timing of the exit out of Africa and the routes taken remain controversial. Archaeological and genetic evidence (Cavalli-Sforza et al. 1994) support two dispersals from Africa. A southern migration that coasting Asia reached Australia, and a northern migration that reached Western Asia through the Near East. Studies based on complete mitochondrial DNA sequences indubitably demonstrated that only two macrolineages, M and N, comprise all the mitochondrial variation existing out of Africa (Ingman et al. 2000; Maca-Meyer et al. 2001; Herrnstadt et al. 2002). Based on the phylogeographic distribution of these two lineages and their derivates, with N prevalent in Europe and western Asia and M more frequent in southern and eastern Asia, we proposed that M and N were the mitochondrial signals of the southern and northern routes respectively (Maca-Meyer et al. 2001). Recently, Palanichamy et al.(2004) disregarded our interpretation as simplistic and, based on new mitochondrial genome data of macrohaplogroup N in India, supported the more parsimonious hypothesis of a single migration route out of Africa proposed by others (Forster et al. 2001), but with the addition of another lineage, R, to that migration. So a scenario with a single migration route out of Africa and three-founder mtDNA lineages was defined. In a recent article(Tanaka et al. 2004) the weakness of both hypothesis to congruently incorporate new mitochondrial data, mainly from Australia and Papua New Guinea (Ingman and Gyllensten 2003), was discussed suggesting that a new work hypothesis should be formulated to accomodate this recent information. Of main concern was the presence, in high frequencies, of macrohaplogroup N basal lineages in aboriginal Australians contrasting with its paucity in India and its absence in PNG. If, as we proposed, N marks the northern route, how to explain its absence in southeast Asia and PNG, its natural path to Australia? On the other hand, if N was carried along with M in all routes how to explain its paucity in India and its absence in southeast Asia? Not to mention the lack of basal M in western Eurasia. In accordance, we have now modified our previous hypothesis. In this second version we continue proposing at least two successive migrations from Africa. Anthropological studies show that Palaeolithic humans most probably moved in small groups with close familiar ties. This endogamic structure induces loss of variation. So we think improbable that two divergent lineages such as M and N, separated by nine independent point mutations, were simultaneously carried by only one of those small groups. In relation to R, it is a macro-haplogroup that comprises all the N lineages characterized by the reversion of 16223 and the presence of the 12705 substitution. So, it is phylogenetically derived from the basal N. Until now, no authochtonous derived N lineages have been detected in Africa. Therefore, we suppose that R arose out of Africa. It might be argued that the coalescence ages of the three macro-haplogroups are similar but the errors of these dates are so large that simultaneous or successive departures from Africa fit in them as well.

Now we think that the first successful group of modern humans leaving Africa mainly carried basal N lineages. Their spread out of Africa was global. Climatic conditions should not have been insurmountable for groups that chose North, whereas others moved eastwards. R could have appeared before this split, going with N in both routes or, most probably, arose in the northern branch. With time offshots of this northern trunk colonized Europe westwards, India southwards and, going eastwards, reached Northeast and Southeast Asia including PNG where R lineages have been detected (Ingman and Gyllensten 2003).

Relatively short in time, the second out of Africa human wave carried mainly basal M lineages. The lack of primitive M lineages in Europe and Central Asia suggests that this second migration found climatic dificulties to spread northwards or was adapted to exploit mainly marine resources choosing therefore a coastal migration (Stringer, 2000). The southern route of M most probably followed the track of their N precursors, displacing and nearly substituting them in India and hastened their trail to Australia in spite of the maritime barriers found in this exodus. M could have reached Australia following N but, most probably continued eastwards colonizing Southeast Asia and PNG originating, from this area, a second migration to Australia. The independent histories of the human Y chromosomes from Melanesia and Australia (Kayser et al. 2001) are more in accordance with this second alternative.

We understand that the data in support of our hypothesis are meager at best. However, it explains the currently observed geographic patterns of mtDNA variation fairly well. Of course, recurring to genetic drift and lineage extinctions other stories may also fit the present mtDNA phylogeography. In any case, it is indispensable that any hypothesis can be testable. Studies of mitochondrial variability in southern and northern areas of India for R lineages could help to define the gate of entrance of this macro-haplogroup in India. RFLPs distinguishing M from N lineages could be performed on the most ancient remains of aboriginal Australians to confirm that really these first immigrants belonged to macrohaplogroup N. The same type of study applied to sinodont and sundadont Chinese remains would give information of their mtDNA adscription.

Finally, as predictably new N and R lineages will be detected in future studies of Southeast Asia and Oceania, we would like to suggest that those N and R lineages already found in Australia and PNG be named according to the widely accepted nomenclature system of Richards et al. (1998).

References

Cavalli-Sforza LL, Menozzi P, Piazza A: The history and geography of human genes. New Jersey: Princeton University Press; 1996.

Forster P, Torroni A, Renfrew C, Röhl A: Phylogenetic star contraction applied to Asian and Papuan mtDNA. Mol Biol Evol 2001, 18:1864-1881.

Herrnstadt C, Elson JL, Fahy E, Preston G, Turnbull DM, Anderson C, Ghosh SS, Olefsky JM, Beal MF, Davis RE, Howell N: Reduced-median-network análisis of complete mitochondrial DNA coding-region sequences for the major African, Asian, and European haplogroups. Am J Hum Genet 2002, 70:1152-1171.

Ingman M, Kaessmann H, Pääbo S, Gyllensten U: Mitochondrial genome variation and the origin of modern humans. Nature 2000, 408:708-713.

Ingman M, Gyllensten U: Mitochondrial genome variation and evolutionary history of Australian and New Guinean aborigines. Genome Res 2003, 13:1600-1606.

Kayser M, Brauer S, Weiss G, Schiefenhövel W, Underhill PA, Stoneking M: Independent histories of human Y chromosome from Melanesia and Australia. Am J Hum Genet 2001, 68:173-190.

Maca-Meyer N, González AM, Larruga JM, Flores C, Cabrera VM: Major genomic mitochondrial lineages delineate early human expansions. BMC Genetics 2001, 2:13.

Palanichamy MG, Sun C, Agrawal S, Bandelt H-J, Kong Q-P, Khan F, Wang C-Y, Chaudhuri TK, Palla V, Zhang Y-P: Phylogeny of mitochondrial DNA macrohaplogroup N in India, based on complete sequencing: Implications for the peopling of South Asia. Am J Hum Genet 2004, 75:000-000

Richards M, Macaulay V, Bandelt H-J, Sykes B: Phylogeography of mitochondrial DNA in western Europe. Ann Hum Genet 1998, 62:241-260.

Tanaka M, Cabrera VM, González AM, Larruga JM, Takeyasu T, Fuku N, Guo L-J, et al Mitochondrial genome variation in eastern Asia and the peopling of Japan. Genome Res 2004, 14:1832-1850.

Stringer C: Coasting out of Africa. Nature 2000, 405:24-27.

Competing interests

None declared

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