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Human evolution: The southern route to Asia
Todd R. Disotell

Research on human origins has tended to focus on the origins of western Eurasians; only recently have genetic studies examined south and east Asian populations in depth. Recent work suggests that the supposed Aryan invasion of India 3,000–4,000 years ago was much less significant than is generally believed.
Address: Department of Anthropology, New York University, 25 Waverly Place, New York, New York 10003, USA. Current Biology 1999, 9:R925–R928 0960-9822/99/$ – see front matter © 1999 Elsevier Science Ltd. All rights reserved.

analysis of a large sample of south Asian mitochondrial (mt)DNA sequences and recent discoveries of previously unknown mtDNA types in Ethiopia. The initial mtDNA study of Cann et al. [6] and subsequent studies have found far greater genetic variation within Africa than in the rest of the Old World, consistent with the view that the African population as a whole originated between 100,000 and 200,000 years ago, and that the dispersal outside of Africa occurred much less than 100,000 years ago [7,8]. Population differentiation thus probably occurred for a considerable period within Africa before populations dispersed elsewhere into the Old World [9]. One of the weaknesses of many genetic studies of modern human origins is the difficulty of both carrying out and interpreting phylogenetic analyses. The most widely used technique for inferring evolutionary relationships from genetic sequence data is maximum parsimony. This technique calculates the number of evolutionary events — nucleotide substitutions in the case of DNA sequences — over all possible bifurcating trees linking the samples being analyzed. As many tree topologies may require the same number of events, multiple equally parsimonious trees are often found. This is especially true for large data sets or those in which only a few differences exist between the various samples. If some of the changes shared between individuals have arisen independently — known as homoplasies — maximum parsimony approaches may give misleading results. An alternative approach to inferring phylogenies from intraspecific data, which often consist of large samples with small distances between individuals, is the ‘medianjoining’ technique recently put forth by Bandelt et al. [10]. This method creates a network out of data for non-recombining parts of the genome, such as mtDNA or Y chromosome sequences, by joining individuals who differ by only a specified number of changes into clusters, which themselves are linked to other clusters and the network as a whole (Figure 1). This method can tolerate a reasonable amount of homoplasy. Instead of finding tens of thousands of equally parsimonious trees with little resolution, the median-network approach will produce a single network with alternative potential evolutionary paths between individuals and clusters of individuals [10] (Figure 1). It is this method that Kivisild et al. [5] have used to effect in their study of the origins of Indian populations. While a great deal of research effort has focused on the origins of Europeans and the fate of the neanderthals,

According to the multiregional model of human evolution, archaic humans originated in Africa, migrated throughout the Old World over a million years ago, and then evolved into modern form multiple times in different areas of the Old World, with enough gene flow between these regions to prevent speciation [1]. In this scenario, east Asians, Australians, Europeans and Africans would each have had relatively ancient separate ancestries. This theory is supported predominately by paleoanthropologists who see, for instance, that “the hominid fossils from Australasia (Indonesia, New Guinea and Australia) show a continuous anatomic sequencing during the Pleistocene that is un-interrupted by African migrants at any time” [1]. Southeast and south Asian populations are also often thought to be derived from the admixture of various combinations of western Eurasians (‘Caucasoids’), east Asians and Australasians. The combinations of phenotypic traits in some of these populations could then be viewed either as the results of such admixture, or as traits selected for a particular environment (for example dark skin). The widely supported recent replacement model, on the other hand, posits a relatively recent African origin for all modern humans, with a subsequent dispersal throughout the Old World that completely replaced the existing archaic population (reviewed in [2]). A model with a single migration out of Africa, however, is receiving less support as additional fossil and genetic studies more fully characterize human diversity, both past and present. Several researchers [3,4] have proposed that two geographical routes were taken by early modern migrants from Africa: a ‘northern’ route through north Africa and the Middle East towards western Eurasia, and a ‘southern’ route through Ethiopia and the Arabian peninsula towards South Asia. A study recently published in Current Biology [5] provides important new support for the ‘southern’ route hypothesis, from the

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Figure 1 On the left is shown a strict consensus tree of the numerous equally parsimonious trees linking 14 mtDNA types from a sample of 61 humans [16]. On the right is shown the median–joining network linking the 14 mtDNA types with one change between each node (after [10]). Note type H14 could be derived from either H1 or H8 and type H10 from either H1 or H7. Additional information, based on geography and from other studies, suggests that the links represented by the grey lines are less plausible [10].

H3 H6 H11 H13 H10 H14 H12 H1 H2 H3 H4 H5 H6 H7 H8 H9 H14

H12

H1

H10

H9

H8 H5

H2

H7

H4 H11

H13
Current Biology

surprisingly few studies have examined large samples from Asian and Australian populations. For instance, the patterns of genetic diversity in India — soon to be home to the world’s largest population — have only recently come under scrutiny using the latest molecular and analytical techniques. Kivisild et al. [5] have now reported a study that includes an analysis of 550 Indian mtDNA samples using the median-joining approach. All of the Indian mtDNA types found could be derived from the African mtDNA haplogroup L3a, which is of course consistent with an African origin, and if the timing is right, with the recent replacement hypothesis. (A haplogroup is a cluster of mtDNA types consisting of closely related sequences that differ by only a few nucleotide substitutions.) They found that 60% of Indian mtDNA types belong to the Asian-specific haplogroup M. Kivisild et al.’s [5] large scale study also found that the mtDNA haplogroup U, until now thought to be a western Eurasian marker based on much smaller studies, is the second most frequent type in India, with a 20% frequency. This haplogroup is actually composed of seven subtypes: the western Eurasian subtypes are found at a low frequency in India, and vice versa. The ‘coalescence’, or time of origin, for the western Eurasian and Indian U2 subtypes was calculated as 53,000 years ago. Another haplogroup, U7, found at much higher frequencies in India and rarely in western Eurasia, has an estimated coalescence date of 32,000 years ago. Where western Eurasian mtDNA types are found among the Indian sample, their frequencies are more than ten times lower than in western Eurasia. Within these shared types, the divergence times between Indian and western Asian types — estimated from the minimal distances between their corresponding mtDNA hypervariable

region sequences and a reasonable mutation rate — is on the order of 9,000 years ago, which Kivisild et al. [5] interpret as indicative of a small amount of admixture, possibly due to the expansion of agricultural populations from the fertile crescent. These findings, coupled with the recently discovered presence of haplogroup U in Ethiopia [11], support a scenario in which a northeast African population dispersed out of Africa into India, presumably through the Arabian peninsula, before 50,000 years ago (Figure 2). Other migrations into India also occurred, but rarely from western Eurasian populations. The supposed Aryan invasion of India 3,000–4,000 years before present therefore did not make a major splash in the Indian gene pool. This is especially counter-indicated by the presence of equal, though very low, frequencies of the western Eurasian mtDNA types in both southern and northern India. Thus, the ‘caucasoid’ features of south Asians may best be considered ‘pre-caucasoid’ — that is, part of a diverse north or north east African gene pool that yielded separate origins for western Eurasian and southern Asian populations over 50,000 years ago. Recent large scale genetic studies of east Asian and Australasian populations are consistent with this scenario. Chu et al. [12] typed from between 15 and 30 microsatellites in 28 Chinese populations as part of the Chinese Human Genome Diversity Project. They inferred that the genetic data do not support an independent origin of modern humans in China, as proposed by the multiregional model, but rather that the ancestors of the Chinese dispersed from south eastern Asia. Thus, rather than being an ancient population that intermixed with other populations at its periphery, especially to the south, the far east Asian population may be relatively recently derived from south

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Figure 2 The ‘northern’ (green) and ‘southern’ (red) human dispersal routes inferred from patterns of mtDNA variation. According to Kivisild et al. [5], the more recent 9,000 year old dispersal from the fertile crescent region into southern and eastern Asia (blue) provided a very minor contribution to Asian mtDNA gene pools (see text for details).

53,000 years

9,000 years 53,000 years >30,000 years

>40,000 years

Current Biology

east Asian ancestors, who themselves are derived from populations dispersing from the Indian subcontinent just over 50,000 years ago (Figure 2). One of the more perplexing questions about modern human evolution centers around the origins of the aboriginal Australians and other people of the Sahul — the Pleistocene landmass that connected Australia, New Guinea, Tasmania and many of the islands in the region. Archeological evidence suggests that Australia was colonized between 40,000 and 60,000 years ago [13]. If the multiregional model is ruled out, and the million or so year old archaic inhabitants of the region did not leave their genes behind, as most molecular evidence suggests, where did these populations come from? Conflicting hypotheses have been proposed based on multiple genetic data sets and types of analysis. Multiple migrations and dispersals probably further confound these analyses. Some recent mtDNA-based studies (for example [14]) link Australian aborigines with populations from New Guinea, though perhaps with several migration events leading to distinct subgroups on each island. Other studies have found a link between the Australians, but not New Guineans, and Indian populations [15]. Hypervariable sites in the most commonly sequenced region of the mitochondrial genome make the application of tree-based comparisons to global samples particularly difficult, even for median-joining approaches [14]. Estimating coalescence dates is also problematic for these populations, perhaps because of increased genetic drift as a result of their relative isolation. Despite the confusion as to from where and when Sahulian populations are derived — south Asia, south east Asia or perhaps both — a scenario in which they are ultimately derived from an African pop-

ulation who dispersed by the ‘southern route’ within the last 60,000 years is becoming increasingly likely (Figure 2). This scenario could also explain one of the enduring mysteries of human morphological variation. South Asian populations are typically classified as ‘caucasoid’, despite numerous phenotypic features that resemble Africans and Australian aborigines. These may be ancestrally retained ‘pre-caucasoid’ traits derived from a north or north-east African population before the western Eurasian/south and east Asian divergence. The darkskinned Australian aborigines, who often cluster with some African populations when morphometric comparisons of skulls are made, may also share many ancestral traits with the original founding population. Various Indian Ocean and Pacific island populations often display a constellation of ‘negrito’ traits, including small stature, dark skin and tightly curled hair. Usually, these traits are explained as evolving due to a combination of mutation, isolation, drift, and selection to tropical environments over hundreds of thousands of years. If the ‘southern route’ scenario is correct, these traits may be the results of selection of a quite variable population that expanded along the southern periphery of the Asian continent relatively rapidly between 50,000 and 60,000 years ago. Rather than being perplexed by these features, it is clear that they need to be reevaluated in light of the evidence supporting such a scenario.
References
1. Thorne AG, Wolpoff MH: The multiregional evolution of humans. Sci Am 1992, 266:76-83. 2. Disotell TR: Origins of modern humans still look recent. Curr Biol 1999, 9:R647-R650. 3. Cavalli-Sforza LL, Menozzi P, Piazza A. The History and Geography of Human Genes. Princeton, New Jersey: Princeton University Press; 1994.

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4. Lahr MM, Foley R: Multiple dispersals and modern human origins. Evol Anthrop 1994, 3:48-60. 5. Kivisild T, Bamshad MJ, Kaldma K, Metspalu M, Metspalu E, Reidla M, Laos S, Parik J, Watkins WS, Dixon ME, et al.: Deep common ancestry of Indian and western Eurasian mtDNA lineages. Curr Biol 1999, 9:1331-1334. 6. Cann RL, Stoneking M, Wilson AC: Mitochondrial DNA and human evolution. Nature 1987, 325:31-36. 7. Watson E, Forster P, Richards M, Bandelt H-J: Mitochondrial footprints of human expansions in Africa. Am J Hum Genet 1997, 61:691-704. 8. Mountain JL, Hebert JM, Bhattacharyya S, Underhill PA, Ottolenghi C, Gadgil M, Cavalli-Sforza LL: Demographic history of India and mtDNA-sequence diversity. Am J Hum Genet 1995, 56:979-992. 9. Harris EE, Hey J: X chromosome evidence for ancient human histories. Proc Natl Acad Sci USA 1999, 96:3320-3324. 10. Bandelt H-J, Forster P, Röhl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999, 16:37-48. 11. Passarino G, Semino O, Quintana-Murci L, Excoffier L, Hammer M, Santachiara-Benerecetti AS: Different genetic components in the Ethiopian population, identified by mtDNA and Y-chromosome polymorphisms. Am J Hum Genet 1998, 62:420-434. 12. Chu JY, Huang W, Kuang SQ, Wang JM, Xu JJ, Chu ZT, Yang ZQ, Lin KQ, Li P, Wu M, et al.: Genetic relationship of populations in China. Proc Natl Acad Sci USA 1999, 95:11763-11768. 13. Klein RG: The Human Career: Human Biological and Culture Origins 2nd ed. Chicago: University of Chicago Press, 1999. 14. van Holst Pellekaan SM, Frommer M, Sved JA, Boettcher B: Mitochondrial control-region sequence variation in Aboriginal Australians. Am J Hum Genet 1998, 62:435-449. 15. Redd AJ, Stoneking M: Peopling of Sahul: mtDNA variation in Aboriginal Australian and Papua New Guinean populations. Am J Hum Genet 1999, 65:808-828. 16. Nachman MW, Brown WM, Stoneking M, Aquadro CF: Nonneutral mitochondrial DNA variation in humans and chimpanzees. Genetics 1996, 142:953-963.

If you found this dispatch interesting, you might also want to read the December 1999 issue of

Current Opinion in Genetics & Development
which included the following reviews, edited by Phil Green and Eugene Koonin, on Genomes and evolution:
Comparative genomics and evolutionary biology Alexy S Kondrashov Orthologs, paralogs and genome comparisons J Peter Gogarten and Lorraine Olendzenski Coding sequence evolution Martin Kreitman and Josep M Comeron Selfish operons: the evolutionary impact of gene clustering in prokaryotes and eukaryotes Jeffrey Lawrence Shaping the genome - restriction-modification systems as mobile genetic elements Ichizo Kobayashi, Ayaka Nobusato, Noriko KobayashiTakahashi and Ikuo Uchiyama Interspersed repeats and other mementos of transposable elements in mammalian genomes Arian FA Smit Insights into the evolutionary process of genome degradation Jan O Andersson and Siv GE Andersson The nature of the last universal common ancestor David Penny and Anthony Poole Evolution of organellar genomes Michael W Gray Origin of multicellular eukaryotes - insights from proteome comparisons L Aravind and G Subramanian Noncoding RNA genes Sean R Eddy Contribution of genomics to bacterial pathogenesis Dawn Field, Derek Hood and Richard Moxon The genome of the malaria parasite Malcolm J Gardner The minimal genome concept Arcady Mushegian Observing the living genome Tracy L Ferea and Patrick O Brown The full text of Current Opinion in Genetics & Development is in the BioMedNet library at
http://BioMedNet.com/cbiology/gen

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