natives or immigrants: modern human origin in east asia

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NATIVES OR IMMIGRANTS: MODERN HUMAN ORIGIN IN EAST ASIA Li Jin and Bing Su East Asia is one of the few regions in the world where a relatively large number of human fossils have been unearthed — a discovery that has been taken as evidence for an independent local origin of modern humans outside of Africa. However, genetic studies conducted in the past ten years, especially using Y chromosomes, have provided unequivocal evidence for an African origin of East Asian populations. The genetic signatures present in diverse East Asian populations mark the footsteps of prehistoric migrations that occurred tens of thousands of years ago. ALLOZYME

A different electrophoretic form of the same enzyme due to allelic differences.

Human Genetics Center, University of Texas, Houston, Texas 77030, USA. School of Life Sciences, Fudan University, China. National Human Genome Center at Shanghai, China. e-mails: [email protected]; [email protected]

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The ‘Out-of-Africa’ hypothesis of modern human origins suggests that local populations outside Africa were completely replaced by modern humans who originated in Africa. This hypothesis has been widely accepted since it was first proposed in the late 1980s, and it is supported by extensive genetic evidence and by archaeological findings1–8 (see BOX 1 for the competing hypotheses9,10). However, it has been claimed, mostly by archaeologists, that the abundant hominid fossils found in China and in other regions of East Asia show evolutionary continuity, not only in morphological characters, but also in spatial and temporal distributions11–14. This observation implies that the evolution from Homo erectus to Homo sapiens and then to Homo sapiens sapiens (modern man), took place in East Asia as well as in Africa — a theory that has been used repeatedly to challenge the validity of the Out-ofAfrica hypothesis13,14. Genetic data that support the Out-of-Africa model, which come mostly from mitochondrial DNA (mtDNA) studies, are often disputed, and the interpretation of the genetic evidence has been controversial15–20. Furthermore, in most of the genetic studies, the Chinese DNA samples derive from Canton, in Southern China, which contains many diversified ethnic populations. Therefore, this might not be the representative sample needed to resolve the competing hypotheses of modern

human origin in East Asia3–6. In addition, although the expansion of modern humans into Europe, the Americas and Oceania (Australia and New Guinea) is now relatively well characterized17, little is known about the earliest migratory routes that modern humans took in spreading from Africa to Asia. So a close examination of East Asians is essential to resolve the long-standing controversy over the origin of modern humans. A recent series of genetic studies on East Asian populations have been informative. The results have filled the gap in the genetic data of this important region, and have cleared the confusion that surrounds the origin and prehistory of humanity in East Asia7,21,22. Genetic relationship of East Asian populations

The genetic structure of Chinese populations was first studied using classical genetic markers, such as blood groups, immunoglobins and ALLOZYMES23–25. A distinct genetic difference was observed between northern and southern populations, despite millennia of common history and migrations. This raises the question of whether southern and northern populations are descendants of the same population or belong to populations that arrived in China from different sources. Several studies of mtDNA variations in a limited number of populations indicated that East Asians may descend from a common ancestor26–28. The mtDNA

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Box 1 | ‘Out-of-Africa’ versus the multiregional hypothesis A

B

C

D

1,000,000 H. erectus years ago

100,000 H. s. sapiens years ago

Africa

Europe

Asia

Oceania

Broadly speaking, there are two competing hypotheses on the origin of modern humans: the Out-of-Africa hypothesis and the multiregional hypothesis (reviewed in REFS 9,10). Both agree that Homo erectus originated in Africa and expanded to Eurasia about one million years ago, but they differ in explaining the origin of modern humans (Homo sapiens sapiens). The first hypothesis proposes that a second migration out of Africa happened about 100,000 years ago, in which anatomically modern humans of African origin conquered the world by completely replacing archaic human populations (Homo sapiens) (Model A). The multiregional hypothesis states that independent multiple origins (Model D) or shared multiregional evolution with continuous gene flows between continental populations (Model C) occurred in the million years since Homo erectus came out of Africa (the trellis theory). A compromised version of the Out-of-Africa hypothesis emphasizes the African origin of most human populations but allows for the possibility of minor local contributions (Model B).

GENETIC ARCHITECTURE

The genetic make-up of a population. HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY

A technique for separating DNA or protein molecules by molecular weight and conformation. VARIANCE

A measure of the variation around the central class of a distribution (the average squared deviation of the observations from their mean value). ASCERTAINMENT BIAS

An error introduced with a biased sampling scheme. HAPLOTYPES

A set of genetic markers present on one chromosome.

data from seven Asian populations28 are consistent with the hypothesis of a common southern origin of East Asians, which had originally been proposed on the basis of dental variations29. In 1998, Chu et al. studied the GENETIC ARCHITECTURE of East Asians using up to 28 East Asian populations and 30 autosomal-microsatellite markers7. By using an approach based on the phylogenetic relationships between populations, they showed that all East Asian populations in their study form a single cluster rooted by African populations. This observation strongly supports a common African origin of East Asian populations. In addition, northern and southern East Asians belong to distinct clusters in the phylogenetic tree, confirming that they are genetically divergent. The phylogenetic analysis also indicated that the peopling of East Asia might have been caused by an entry of modern humans from the south, followed by a northward migration. This was the first systematic genetic study on East Asian populations and provided the genetic evidence that supports the Out-of-Africa origin of modern humans of East Asia30. However, the phylogeny presented in this study has relatively weak statistical support and falls short of providing an unequivocal picture of the prehistoric migrations of modern humans in that region.

Several studies using other autosomal and X-chromosomal markers in worldwide populations are also consistent with the Out-of-Africa hypothesis4,6,31–33. However, as only a few East Asian populations were analysed, there is insufficient data to refute the multiregional hypothesis convincingly, let alone trace the early migrations of modern humans in East Asia. A recent study of the markers on chromosome 21 provided encouraging evidence by using intact autosomal haplotype data to trace migrations34. A 565-base-pair DNA fragment near the MX1 gene (which encodes an interferon-inducible protein) was found to contain nine polymorphic sites in human populations. No recombination or recurrent mutations (for example, A→G and then back to A) were observed in this genomic region. The results show that Africans have the greatest overall haplotype diversity. The ancestral haplotype (called Ht1) has moderate frequency in African populations, but is rare or absent in other world populations, including five East Asian populations. This finding is consistent with the Out-of-Africa hypothesis34. Y-chromosome haplotypes

In 1999, another systematic genetic study on East Asian populations was published by Su and colleagues21. A set of 19 highly informative Y-chromosome biallelic markers, developed at Stanford University, were used to reveal the genetic structure of the paternal lineages in East Asia (BOX 2). Owing to the low level of genetic diversity, the use of Y-chromosome markers in reconstructing human history35 had been hampered until the introduction of denaturing HIGH-PERFORMANCE LIQUID CHROMATOGRAPHY, an efficient technique for detecting mutations36–38. Many Y-chromosome biallelic markers have been identified in the past few years36,39,40. Su et al.21 studied a large collection of population samples, including 21 Chinese ethnic populations, 22 provincial Han Chinese populations, three Northeast-Asian populations and five Southeast-Asian populations, as well as 12 non-Asian populations from Africa, America, Europe and Oceania. These representative samples and the informative Y-chromosome markers led to the conclusion that Southeast-Asian populations are much more diverse than their northern counterparts, and could mean that mainland Southeast Asia was the first settlement of modern humans in East Asia. On the basis of the VARIANCE of Y-chromosome microsatellites, the initial settlement was estimated to have occurred 18,000–60,000 years ago. It was hypothesized that a northward diaspora, coinciding with the retreating glacier of the last ice age, resulted in the peopling of China and of northerly regions as far as Siberia21. The current genetic difference between northern and southern East Asian populations was probably caused by a bottleneck event that occurred during the northward migration, followed by geographic separation21,41. The original set of samples used for screening is highly representative of both northern and southern East Asian populations, and excludes possible ASCERTAINMENT BIAS. In addition, the distribution patterns of the HAPLOTYPES shared by multiple populations reveal regional characteristics, thereby

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1

2

M130 (C→T)

M89 (C→T)

M1 (Alu insertion)

M9 (C→G)

M122

M119

M95

M5

M45

M15 M7

African ancestors

M134

M50 M103 M110

M3

M88 M120

M117

M111

H1 H2 H3 H4 H7 H6 H8 H9 H10 H11 H12 H5 H17 H13 H14 H15 H16

Figure 1 | The phylogeny of Y-chromosome haplotypes in East Asians (H1–H17). The Ychromosome haplotypes H1–H17 are observed in East Asian populations21,22. East Asianspecific haplotypes (H6–H12) are indicated in red. The genetic loci associated with the haplotypes are labelled next to the branches, and the polymorphisms at these loci are indicated in brackets. The shaded region represents the work in REFS 21,22. On the basis of this work, the ancestral haplotype, H1, is indistinguishable from African haplotypes. Mutations 1 and 2 are two ancient polymorphisms (point mutations)40. Mutations 1 and 2 establish that H1 is actually derived from African haplotypes.

GENETIC DRIFT

Changes in allele frequency that result because the genes appearing in offspring are not a perfectly representative sample of the parental genes (for example, in small populations). ALU SEQUENCE

A dispersed, intermediately repetitive DNA sequence found in the human genome in about 300,000 copies. The sequence is about 300 base pairs long. The name Alu comes from the restriction endonuclease (AluI) that cleaves it. EFFECTIVE POPULATION SIZE

The size of a population determined by the number of individuals who contribute to the next generation, assuming random mating.

128

chromosome Alu polymorphism; M1 in FIG. most East Asian Y chromosomes (H2–H17) can be traced back to an African ancestor. However, as the East Asian individuals that carry H1 (about 10%) are ancestral to all the other haplotypes, and are therefore indistinguishable from those in Africans21, these could conceivably be carrying Y-chromosomal lineages that represent a local origin. Recently, up to 98 new Y-chromosomal simplesequence polymorphisms (point mutations and short insertions or deletions) were reported in the coding and the flanking non-coding regions of four Y-chromosome genes39,40. They reveal an extreme geographic structure, with the oldest clades representing African populations and the younger ones representing some African and all non-African populations. In other words, the nonAfrican Y chromosomes seem to be derived from a small number of Africans. Thomson et al.39 estimated the age of the common ancestor of the Y chromosomes to be 59,000 years (95% confidence interval: 40,000–140,000 years) if based on the assumption of recent population growth, or 84,000 years (95% confidence interval: 55,000–149,000 years) if a constant population size is assumed. The recent common African ancestry is therefore a strong confirmation of the Outof-Africa hypothesis. In contrast, the clear geographic structure was not observed in the mtDNA data1,3 owing to frequent recurrence of mutations, which tends to blur the geographic pattern, or possibly because of the larger EFFECTIVE POPULATION SIZE of mtDNA compared with that of the Y chromosome (BOX 2). Two critical point mutations, defined as mutations 1 and 2, are believed to be associated with the Out-ofAfrica migratory event. When the East Asian data are incorporated into the global tree, all the haplotypes found in East Asia (including H1) fall into the younger clade unified by mutation 2. This mutation is derived from mutation 1 (REF. 40), which is only polymorphic in Africa40 (FIG. 1). Therefore, all 1,046 Y chromosomes21,22 sampled from East Asia are directly derived from the African lineages. With these data, the replacement of modern humans of African origin in East Asia is complete. This leaves the multiregional hypothesis only a remote possibility (in East Asia, at least), although a larger sample may be needed to establish this with stronger confidence. 1)5.Therefore,

reducing the bias that might be introduced by sampling errors or from GENETIC DRIFT. Of the haplotypes derived from the 19 Y-chromosome biallelic markers, 17 are present in more than 1,000 East Asian individuals from different ethnic backgrounds. No recurrent mutations were observed and the phylogenetic relationships among the haplotypes are unequivocal owing to the non-recombinant nature of Y chromosomes (FIG. 1). Therefore, the geographic distribution (see FIG. 2 for the geographic locations of populations sampled) of these 17 haplotypes reflects the demographic history of the populations under study. H1 is the ancestral haplotype and H2–H17 are the derived haplotypes. The majority (about 70%) of East Asian Y chromosomes (H6–H12) are specific to East Asians and absent in other world populations, indicating a common origin of East Asian populations (FIG. 2). Those haplotypes specific to East Asians share a C→G mutation at locus M9 that is also prevalent in other world populations, except those in Africa36. H5 and H13–H17 also belong to this lineage. H4 was derived from H1, but is ancestral to the M9G haplotypes (H5–H17) and is defined by a C→T mutation at locus M89. This mutation has a non-trivial contribution (roughly 4% on average) to East Asians, especially to northerners (for example, 20% in Hui, 11% in Manchurians and 8.3% in Mongolians). The H2 and H3 haplotypes, which are predominant in Tibetan and Japanese populations but are generally absent in other East Asians, contain an insertion of a 300-base-pair ALU SEQUENCE, or YAP (Y-

Genetic and archaeological data

The Out-of-Africa hypothesis has been subjected to two main criticisms from the school of multiregionalists. The first is the claim that the multiregional hypothesis has been misinterpreted, by suggesting that it demands that modern populations have strictly independent origins. According to the network (trellis) model, frequent gene exchanges would have occurred between continental populations since H. erectus came out of Africa about one million years ago, causing shared multiregional evolution across the human range (BOX 1)42. It was claimed that the extensive genetic data supporting the Out-of-Africa hypothesis could also be explained under this version of the multiregional hypothesis. However,




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COALESCENCE

A pedigree-like network in which all living individuals sampled are united under a most recent common ancestor.

million years)43. This difference in age estimates might only reflect the difference in the effective population sizes between Y chromosome/mtDNA and X chromosome/autosome (3–4 times greater in the latter) in bottleneck events that were associated with the outbound migrations from Africa44. That is, the COALESCENCE of autosome and X chromosome DNA sequences may precede the divergence between Africans and nonAfricans. In other words, the age estimates based on Xchromosomal and autosomal regions are compatible with both competing hypotheses; therefore, those above are not useful statistics to distinguish between the two competing models. The second argument raised by multiregionalists comes from archaeological findings in East Asia, especially in China. As already mentioned, a continuous evolutionary chain has been proposed to connect H. erectus to H. sapiens in China, and this was used to support either an independent origin of modern humans in East Asia or the trellis model11,12. However, close examination of the collection of hominid fossils in China revealed a non-trivial temporal gap between archaic humans (H. sapiens) and modern humans (H. s. sapiens) (BOX 3). All the H. sapiens fossils are at least

the trellis model fails to explain the haplotype data from Y chromosomes. As discussed above, evidence from Ychromosome biallelic markers seems to be consistent only under the Out-of-Africa model, as all of the East Asian haplotypes are regionally specific, are derived from a small number of African ancestors and show no ancient local contributions. In particular, all the mutations found outside Africa are less than 50,000 years old and were derived from Africa40. However, if extensive gene flow had occurred between continental populations during the past one million years, the ancient Ychromosome haplotypes seen in African populations, or even much older haplotypes, would also be expected in East Asia, which seems not to be the case. The only remaining genetic evidence that seems to be irreconcilable with the Out-of-Africa hypothesis comes from several studies on autosomal and X-chromosomal genes31–33. The common ancestor of these genes is estimated to have originated 535,000 to 1,860,000 years ago. This is much older than the age estimates for mtDNA and Y chromosomes, and has been considered to favour a multiregional origin. A recent study on a 10-kilobase non-coding region of chromosome 22 gave a similar estimate (about 1.29

Burya at Ma anc chu uria an Mongolian

Kore ean n

Nortthern n Han

Hui

Japanese

Salla Tujia

Tu

Southern Han

Yao Tibettan

Yi Lahu

She

Bariic Taiwanese Dai

Dong Zhuang Li

Thai

Cambodian Micronesian Malaysian Polynesian Indonesian

=H6

=H7

=H8

=H9

=H10

=H11

=H12

=Others

Figure 2 | The distribution of the seven East Asian-specific Y-chromosome haplotypes. Northern populations are indicated in red text and southern populations in black text. The Yangtze River divides the northern and southern populations. Tibetans are an exception and are classified as northern on the basis of their history. In general, the seven East Asian-specific Y-chromosome haplotypes (H6–H12) represent most East Asian Y chromosomes and support a common African origin (FIG. 1). Mainland Southeast Asia is probably the first settlement of modern humans from Africa, as reflected by the presence of almost all seven haplotypes in Thai and Cambodian populations.




REVIEWS

Box 2 | Molecular markers used in population studies Genetic variations on Y chromosomes are inherited paternally from father to son. The effective population size of Y chromosomes is much smaller than that of the autosomes because of the hemizygous (that is, haploid) nature of the Y chromosome, and mating structure (for example, polygamy). Because of this, many of the Y-chromosome biallelic markers tend to show restricted regional distribution or, in other words, population specificity. Mitochondrial DNA (mtDNA) has been the most frequently studied genetic system, providing the foundation for genetic tools to delineate human history. One drawback of mtDNA is its limited genome size (only 16 kilobases). In addition, there is a bias in the distribution of polymorphic sites along the mtDNA genome; these are rare in coding regions and rich (but with frequent recurrent mutations) in non-coding regions. Unfortunately, no systematic study using mtDNA has been done so far on the extant East Asian populations. Y chromosomes have all the merits of the extensively studied mtDNA; the absence of recombination provides unambiguous lineages and a small effective population size, which tends to generate population-specific markers. Y-chromosome haplotypes derived from multiple biallelic markers can be considered as alleles from a single locus that occurred in an ordered time series, each of which might mark the footprint of a unique migration event. In addition, with a genome size about 4,000 times that of mtDNA (60 megabases, 95% of which is non-recombinant), the Y chromosome contains much more information than mtDNA. Furthermore, the slowly mutating biallelic markers and the highly mutable microsatellite markers allow history to be dissected on different timescales. There are potential problems in using Y-chromosome markers. Selection acting on Y chromosomes will influence estimates of the age of common ancestors. In addition, the Y chromosome is strongly subject to the effects of genetic drift and differential male success in producing offspring, which can affect the haplotype frequency markedly.

100,000 years old, whereas all the H. s. sapiens fossils are less than 40,000 years old (with most between 10,000 and 30,000 years old). In other words, no hominid fossils that can be dated from 100,000 to 40,000 years ago have been found in East Asia. This finding is particularly anomalous given the abundance of either earlier or later fossil records that have been found in this area11,12. The long duration of the temporal discontinuity of the fossil records in China and the distinctive morphological characters of the hominid fossils found before 100,000 years ago and after 40,000 years ago implies that this gap cannot be casually attributed to a ‘missing link’. Instead, the extinction of local archaic humans and the subsequent peopling of modern humans from Africa is thought to be a more reasonable explanation21. Interestingly, this 60,000-year fossil gap coincides with the last ice age, during which modern humans of African origin are thought to have arrived in the southern regions of East Asia21. Ancient migrations of modern humans in Asia

ADMIXTURE

Inter-population gene flow.

130

The validation of the Out-of-Africa hypothesis requires an understanding of the migratory routes of modern humans from Africa to East Asia. One interesting observation related to the prehistoric population movements is the substantial distinction between northern and southern East Asian populations that has been observed in the analyses of both genetic markers and of physical characteristics23–25,41,45,46. Three models have been proposed to interpret this observation. The first model postulates a north-to-south migratory pattern, which led to the ADMIXTURE with Australoids41. The second model sug-

gests a southern origin and northward migration of East Asians7,21. The third model assumes that the ancestors of the northern and southern populations arrived in East Asia separately. From the evidence that has been presented so far, genetic data collected on Y chromosomes and autosomal-microsatellite markers support the second model. According to the distribution of Y-chromosome haplotypes in East Asian populations, southern populations are much more diverse than northern populations (admittedly, this could be due to a bottleneck event that occurred in northern populations). The proposed admixture between the East Asian and Australoids (first model) is less likely, as all seven East Asian specific haplotypes are not present in the nonAustronesian-speaking populations sampled from New Guinea Highlanders and from Melanesia Nasioi (presumably Australoids). In addition, the H17 haplotype, which is exclusive to non-Austronesians, was not observed in East Asians21,22. Most Y haplotypes found in northern populations were derived from a subset of the southern populations, which makes the third model unlikely (although the presence of YAP+ and H4 may indicate a contribution from a migration originating in Central Asia that arrived in East Asia much later). Therefore, the main migratory pattern of modern humans in mainland East Asia is from south to north, which is also indicated by mtDNA evidence28. The East Asian-specific haplotypes show a northward migration, but the other haplotypes are also storytellers. Our further genetic dissection with a new Ychromosome marker47 showed that all the H1 haplotypes in East Asians share a C→T mutation at locus RPS4Y (M130 in FIG. 1). We found that all the RPS4Y→T transitions in East Asia originally entered East Asia from the south and then expanded to the northern part of East Asia (L.J. and B.S., unpublished observations). The RPS4Y→T transition is also present in North American Indians47,48, suggesting that a group of the northward diaspora reached the far north of East Asia and eventually found their way to the New World. However, most Y chromosomes found in the American Indian populations may have come from somewhere other than East Asia. To explore the extent of the northward diaspora in East Asia would require a large study of Y-chromosome markers in Siberian populations. Interestingly, the dental evidence showed that the ‘Sinodont dentition’ (a series of characteristic dental traits in East Asians, such as shovel-shaped incisors) in northern Asian peoples occurred about 20,000 years ago, and a similar dentition pattern, which is ancestral to the Sinodont pattern, predominates among all the Southeast Asian populations29. Another important feature of Y chromosomes in East Asia is reflected in the appearance of YAP+ and of a further ancient polymorphism (C→T at locus M89). The haplotypes associated with these two polymorphisms are H2/H3 (YAP+) and H4 (M89T)21. The prevalence of YAP+ and M89T in Central and Mid-eastern Asian populations (R. S. Wells, personal communication) implies a genetic influence to the East Asian populations from the northwest, possibly starting in




REVIEWS Central Asia. The influence of YAP+ from Central Asia to the East Asian populations is mysterious. In East Asian populations, it was demonstrated that only Tibetans (in the west) and the Japanese (in the east) show high frequencies of YAP+, with a sporadic occurrence in the other East Asian populations5. YAP+ is also absent from Siberian populations48, so forming a huge geographic gap in its distribution in East Asia. Interestingly, besides Tibetans (42.5%)49 and the Japanese (27.6%), another Chinese ethnic minority (Yao-Jinxiu), which lives in southern China, shows a high frequency of YAP+ (50%)21. This might provide a clue for tracing the dispersion of YAP+ Y chromosomes, although more data is needed to solve the YAP puzzle. The distribution of M89T is easier to understand than

that of YAP+; it expanded to many populations in the mainland, with more influence on the northern populations and less on the southern populations, but did not reach island populations such as the Taiwanese and Polynesians. Whether YAP+ and M89T came to East Asia from Central Asia in the same migratory wave needs further investigation. After modern humans from Africa settled in Southeast Asia, other than the proposed northward expansion to China and Siberia, they also migrated southward to explore the new habitats. Y-chromosome biallelic markers again were used to trace the origins of Polynesians22. In this study, mainland Southeast Asia was confirmed as the place of the first settlement of modern humans in East Asia, as it holds almost all the

Box 3 | Fossil records in East Asia Gongwangling, Shaanxi (~1,150 K)

Guojiabao, Yunnan (~1,000 K)

Yuanmou, Yunnan (600–1,700 K)

Homo erectus 600 K

Chenjiawo, Shaanxi (500–650 K)

Homo sapiens (archaic humans) Homo sapiens sapiens (modern humans)

500 K

400 K Zhoukoudian Locality 1, Beijing (230–500 K)

300 K Jinniushan, Liaoning (160–310 K) Dali, Shaaxi (209–230 K)

Changyang, Hubei (174–218 K)

200 K Hexian, Anhui (150–195 K) Tongzi, Guizhou (113–181 K) 100 K

Dingcui, Shanxi (160–210 K)

Chaoxian, Anhui (160–200 K) Maba, Guangdong (129–135 K)

Xujiayao, Shanxi (104–125 K)

Zhoukoudian Locality 4, Beijing (122–171 K)

Hominid fossil gap in China (40–100 K)

40 K Salawusu, Inner Mongolia (33–37 K) 30 K 20 K 10 K

INCA BONES

Supernumerary bones on the skull at lambda, the corner between the two parietal and the occipital bones.

Shiyu, Shanxi (27–30 K) Liujiang, Guangxi (10–30 K)

Wushan, Gansu (38–39 K) Longtanshan, Yunnan (~30 K)

Ziyang, Sichuan (35–40 K) Zhoukoudian, Upper Cave (29–34 K)

Yanjiagang, Heilongjiang (~22 K)

Maomaodong, Guizhou (13–15 K)

China is one of the few regions in the world where ancient hominid fossils have been found. The most ancient human fossils in China can be traced back to as early as 1.7 million years ago (see figure). Since the sensational finding of Homo erectus at Zhoukoudian in the early 1930s, originally called the Peking Man (Homo erectus pekinensis), many other hominids have been unearthed at more than 60 sites13. Archaeologists described a set of morphological traits shared between Homo erectus and Homo sapiens, including shovel-shaped incisors, flat nasal saddle and INCA BONES13. However, the existence of morphological continuity between Homo sapiens and Homo sapiens sapiens is controversial. The figure shows the hominid fossil records found in China. The age estimates (1 K being 1,000 years) and the geographic locations of those fossils are labelled next to the time bars. A non-trivial gap exists between 100,000 and 40,000 years ago, for which there are no hominid fossils.




REVIEWS for two independent migrations, one towards Taiwan and the other towards Polynesia. The latter would have occurred through island Southeast Asia, which was by far the fastest and widest expansion of humans during prehistoric times. The Austronesian languages of the Pacific spread across 10,000 kilometres of coastline and sea within a span of only 1,500 years51. Interestingly, a repeated analysis of the published mtDNA data by Richards et al. is more in line with the hypothesis based on the Y-chromosome data58. The genetic relationship between East Asians (including Austronesian-speaking Pacific Islanders) and Australoids still remains a question. However, data from both Y chromosomes and autosomes have indicated two separate migrations from Africa, one to East Asia and the other to Oceania34,36,40. Conclusions Figure 3 | The putative migratory routes of East Asians of African origin. Migrations that have occurred in the past 60,000 years are indicated by the red arrows. The first entry of modern humans into the southern part of East Asia occurred about 18,000–60,000 years ago, followed by a northward migration. A southern route also started from mainland Southeast Asia, through Malaysia and Indonesia, eventually continuing eastwards to the Pacific Islands. The blue arrows indicate a contribution from Central Asia that arrived in East Asia at a later time. Animated online EXPRESS TRAIN MODEL

A hypothesis that claims a rapid eastward migration of humans starting in Southern China, spreading Austronesian language and the associated Lapita culture through the Pacific islands about 4,000 to 5,000 years ago.

1. 2.

3.

132

East Asian-specific haplotypes. The dominating Ychromosome haplotypes found in the Pacific Islanders, including Polynesians and Micronesians, constitute a small subset of haplotypes found in Southeast Asian populations. More interestingly, the haplotypes found in Taiwanese aborigines are generally absent in Polynesia, whereas a specific type found in Melanesian populations (H17) is also missing in the Polynesian populations. These findings are contrary to the two prevailing hypotheses of Polynesian origins. First, it negates the Taiwan-homeland theory of Polynesian origin that is based on mtDNA studies50–53. The Y-chromosome data, however, do not entirely refute the EXPRESS TRAIN MODEL, which contends the spread of Austronesian language and Lapita culture from Southeast Asia54,55. Second, the Y-chromosome data challenge the Melanesian origin of the Pacific Islanders that is supported by α-globin data56,57. Interestingly, all of the Y haplotypes found in Taiwan and in Polynesia were detected in the mainland Southeast Asian populations. These findings have led to an alternative model for the origins of Polynesians, in which Southeast Asia provided the genetic source

Cann, R. L., Stoneking, M. & Wilson, A. C. Mitochondrial DNA and human evolution. Nature 325, 31–36 (1987). Stringer, C. B. & Andrews, P. Genetic and fossil evidence for the origin of modern humans. Science 239, 1263–1268 (1988). Vigilant, L., Stoneking, M., Harpenden, H., Hawkes, K. & Wilson, A. C. African populations and the evolution of human mitochondrial DNA. Science 253,

4.

5. 6.

On the basis of the genetic evidence generated so far, particularly from Y-chromosome data, modern humans in East Asia have a recent common origin in Africa. It is suggested that the first entry of modern humans into the southern part of East Asia occurred about 18,000–60,000 years ago, and was followed by a northward migration that coincided with the receding glaciers in that area. A southern route also started from mainland Southeast Asia, through Malaysia and Indonesia, eventually continuing eastwards to the Pacific Islands (FIG. 3). It should be noted that the conclusions made on the origin and migrations of modern humans in East Asia are definitely not the end of the story. Many questions are unresolved. Future studies will be directed towards: revealing any genetic contribution from local populations by studying a larger sample of East Asians; delineating the local migratory routes in East Asia that led to the diversified languages spoken in this area (six language families and almost 2,000 individual languages, see LINKS); evaluating the genetic influence of Central Asia on East Asian populations, such as YAP+ and M89T; and reconstructing migratory routes from East Asia to the New World implicated by the C→T transitions at the RPS4Y locus. Finally, we should assess the relationship between East Asians and Australoids. Resolving these questions will lead to a more complete understanding of the evolutionary history of our own species. Links DATABASE LINKS MX1 FURTHER INFORMATION The Ethnologue: Languages of

the World ENCYCLOPEDIA OF LIFE SCIENCES Human evolution:

Overview

1503–1507 (1991). Bowcock, A. M. et al. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368, 455–457 (1994). Hammer, M. F. A recent common ancestry for human Y chromosomes. Nature 378, 376–378 (1995). Tishkoff, S. A. et al. Global patterns of linkage disequilibrium at the CD4 locus and modern human


7.

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