A 2012 paper on the Paleolithic contingent in modern Japanese

Researchers concluded that the genetic contribution of the Jomon is 54.362.3% in Ryukyuans and 23.139.5% in mainland Japanese. Additional data, particularly from East Asia, and further analysis will help to refine these estimates, the authors note.

Yungang He and colleagues report the quantitative analysis of single-letter variants in the genetic code (single nucleotide polymorphisms) in genome-wide data from 94 worldwide populations, in order to infer the origin of the Jomon and to estimate the relative contributions of the Jomon and the Yayoi to the genetic pool in contemporary Japan. Analysis of inferred allele frequencies hints at a Northeast Asian origin for the Jomon.

The Jomon people were the sole inhabitants of the Japanese islands for more than 10,000 years until the isolation ended around 2,000 years ago with the arrival of the Yayoi people, immigrants from the continent, carrying rice farming technology and metal tools. But the genetic contribution of the Jomon to the contemporary Japanese population has been hard to determine because all modern Japanese populations are subject to admixture, or gene mixing, at various levels, and no one of exclusively Jomon ancestry now exists.

The results supports previous anthropological research suggesting that the Yayoi may have been better equipped than the Jomon to acquire sufficient food to feed a larger population, allowing the rapid expansion of the Yayoi and their subsequent dispersal from western Japan to other regions.

Yungang He  et al., Paleolithic Contingent in Modern Japanese: Estimation and Inference using Genome-wide Data Scientific Reports 2, Article number: 355 (2012) doi:10.1038/srep00355

Abstract

The genetic origins of Japanese populations have been controversial. Upper Paleolithic Japanese, i.e. Jomon, developed independently in Japanese islands for more than 10,000 years until the isolation was ended with the influxes of continental immigrants about 2,000 years ago. However, the knowledge of origin of Jomon and its contribution to the genetic pool of contemporary Japanese is still limited, albeit the extensive studies using mtDNA and Y chromosomes. In this report, we aimed to infer the origin of Jomon and to estimate its contribution to Japanese by fitting an admixture model with missing data from Jomon to a genome-wide data from 94 worldwide populations. Our results showed that the genetic contributions of Jomon, the Paleolithic contingent in Japanese, are 54.362.3% in Ryukyuans and 23.139.5% in mainland Japanese, respectively. Utilizing inferred allele frequencies of the Jomon population, we further showed the Paleolithic contingent in Japanese had a Northeast Asia origin.

Introduction

The genetic origins of modern Japanese have been debated and three models are noteworthy1. In the ‘continuity’ model, modern Japanese are considered as direct decedents of Jomon, the inhabitants of Japan in Paleolithic time, while their morphology showed secular changes2. In the ‘admixture’ model, Jomon admixed with the Yayoi, more recent continental immigrants, which is consistent with the rapid changes in morphology and culture which took place synchronically about 2,500 years before present (BP)1,3. In the ‘replacement’ model, Paleolithic Jomon was completely replaced by the continental immigrants (Yayoi) after their arrival4. To date, the ‘admixture’ model is seemingly better supported by the increasing lines of evidence of multiple genetic components found in modern Japanese5,6,7.

The upper Paleolithic populations, i.e. Jomon, reached Japan 30,000 years ago from somewhere in Asia when the present Japanese Islands were connected to the continent8. The separation of Japanese archipelago from the continent led to a long period (13,000 – 2,300 years B.P) of isolation and independent evolution of Jomon9. The patterns of intraregional craniofacial diversity in Japan suggest little effect on the genetic structure of the Jomon from long-term gene flow stemming from an outside source during the isolation10. The isolation was ended by large-scale influxes of immigrants, known as Yayoi, carrying rice farming technology and metal tools via the Korean Peninsula. The immigration began around 2,300 years B.P. and continued for the subsequent 1,000 years5. Based on linguistic studies, it is suggested that the immigrants were likely from Northern China, but not a branch of proto-Korean11.

Genetic studies on Y-chromosome and mitochondrial haplogroups disclosed more details about origins of modern Japanese. In Japanese, about 51.8% of paternal lineages belong to haplogroup O6, and mostly the subgroups O3 and O2b, both of which were frequently observed in mainland populations of East Asia, such as Han Chinese and Korean. Another Y haplogroup, D2, making up 35% of the Japanese male lineages, could only be found in Japan6,12. The haplogroups D1, D3, and D*, the closest relatives of D2, are scattered around very specific regions of Asia, such as the Andaman Islands, Indonesia, Southwest China, and Tibet13. In addition, C1 is the other haplogroup unique to Japan6,12. It was therefore speculated that haplogroups D2 and O may represent Jomon and Yayoi migrants, respectively6. However, no mitochondrial haplotypes, except M7a, that shows significant difference in distribution between modern Japanese and mainlanders5. Interestingly, a recent study of genome-wide SNPs showed that 7,003 Japanese individuals could be assigned to two differentiated clusters, Hondo and Ryukyu, further supporting the notion that modern Japanese may be descendent of the admixture of two different components7.

However, the estimation of contribution of the Paleolithic contingency, i.e. Jomon, to modern Japanese posed a technical challenge since all contemporary populations in Japan were subject to admixture at various levels and the ‘pure’ Jomon no longer exist. The STRUCTURE and similar analysis does provide a solution of estimating the relative contribution of different components in admixed populations when both parental populations are available14,15, but such approach was challenged for its accuracy especially when information on parental populations is incomplete16,17.

In this report, we estimated the relative contribution of Paleolithic inhabitants (Jomon) and more recent immigrants (Yayoi) to modern Japanese, under the assumption of the ‘admixture’ model. This was achieved with only one of the parental populations (Yayoi) was available while another parental population (Jomon) was missing. We also explored the possibility of inferring the genetic origin of Jomon.

Results

Genetic contribution of Jomon in mordent Japanese

With the given two-population admixture model (Figure 1, see Materials and Methods section for details), the contributions of Jomon to Hondo Japanese (JP_ML) and Ryukyuans (JP_RK) were estimated by using genome-wide SNP data. Genotypes of both JP_ML and JP_RK populations were produced in PanAsia SNP project (see S1 of Supplementary file).

Figure 1: Demographic model of population admixture with missing population.

Figure 1

The original genetic donor to Yayoi migration is still controversial, both Korean and Chinese (northern or southern Han) were potential candidates5,18. Since genetic difference exists between northern and southern Han Chinese populations19, we examined the possible contribution of both northern Han Chinese (NH, combining data of CHB in HapMap project and NHan in HGDP) and southern Han Chinese (SH, combining data of CN-SH in PanAsia SNP project and SHan in HGDP) respectively in this study. We also examined the contribution of northern East Asian population by combining data of NH and Korean (NHK, including NH and Korean population named KR-KR in PanAsia SNP project) since previous genetic studies differed on whether Koreans were the only immigrants in period of later Jomon and early Yayoi5. Therefore totally three potential genetic sources (NH, SH and NHK) were evaluated respectively as continental genetic donor.

The estimated contribution of Jomon to modern Hondo Japanese ranges from 0.231 to 0.395 for different donors (Figure 2). The contribution of Jomon (0.231) is the lowest, when NHK (combination of Northern Han and Korean) was taken as the donor, with 95% confidential interval (C.I.) 0.215–0.266. When NH and SH were taken as donors, estimated contributions were 0.395 (C.I. 0.379–0.421) and 0.376 (C.I. 0.344–0.387), respectively. In contrast, Jomon’s contribution in modern Ryukyuans is much greater than that in modern Hondo Japanese, regardless the choice of donors. The estimated contribution are 0.543 (95% C.I. 0.512–0.567), 0.605 (95% C.I. 0.605–0.648) and 0.623 (95% C.I. 0.623–0.671), for NHK, NH, and SH, respectively (Figure 2).

Figure 2: Estimated contributions of Jomon in different genetic scenarios.

Figure 2

Proportions of Jomon’s contribution were marked on y-axis and names of the Asian mainland donors were presented on x-axis. Results based on parameters presented in table 1 were shown in blue columns. Open columns presented estimations from scenarios where Jomon’s Ne is only a half of before. Black bars indicated 95% C.I of the estimations.

Combining lines of evidence from the above results and previous reports on both maternal and paternal lineages, none of the three possible donors can be excluded from the model for peopling of Japan. We therefore averaged the above estimations from all three possible donors to assess the proportion of Jomon contribution in modern Japanese. Thus, in Hondo Japanese, 33.4% of genetic component was derived from Jomon, whereas, 60.5% of its genetic component in Ryukyuans may come from Jomon. These estimations based on autosome data are consistent with previous studies using frequencies of Y haplogoups in modern Japanese populations. In particular, overall frequency of Japanese specific Y lineages, D2 and C1, is about 60% in Okinawa (Ryukyu) and 26.446.2% in Japanese mainland6.

It is likely that the effective population size (Ne) of Jomon was relatively smaller than that of the populations in Asian mainland, because history of agriculture is relatively shorter in Japan Archipelago than that in Asian mainland. We applied our estimation in scenarios that Ne of ancestry Japanese is only a half of the size in aforementioned estimations. The extent evaluation shows the reduced Ne led to only minor changes to the estimations of Jomon contribution (Figure 2). In particular, the estimated contribution with reduced Ne is 0.194 (95% C.I. 0.146–0.220), 0.326 (95% C.I. 0.321–0.356) and 0.369 (95% C.I. 0.356–0.387) for Hondo Japanese and 0.510 (95% C.I. 0.490–0.525), 0.557 (95% C.I. 0.546–0.592) and 0.575 (95% C.I. 0.554–0.602) for Ryukyuans with three possible donors, respectively. In other words, the estimations are robust to the changes of the parameters of demographic model.

Genetic affinity of Jomons

With the genetic contribution of Jomon in Ryukyuans and Hondo Japanese being 33.4% and 60.5% respectively, allele frequencies of SNPs of ancestral Jomon populations were inferred using the maximum likelihood (ML) method described in the Materials and Methods section. Overall allele frequencies in 6 virtual Jomon populations (JOMON ML-NH, JOMON ML-SH, JOMON ML-NHK, JOMON RK-NH, JOMON RK-SH and JOMON RK-NHK) were inferred based on two extant Japanese populations, i.e. Hondo and Ryukyuans, and three possible continental donors including NH, SH, and NHK. The inferred allele frequencies of Jomon populations allowed the reconstruction of the phylogeny including Jomon and the extant populations, using coancestry coefficient20 as the measurement of genetic distance and Neighbor-Joining method (NJ) for phylogeny reconstruction. Interestingly, all six inferred Jomon populations fell into the group of Northeast Asian populations but not that of the populations in South Asia or Southeast Asia (Figure 3A). The results of Principle Component Analysis (PCA) confirmed the genetic affinity shown in the NJ tree (Figure 3B). Jomon is therefore genetically closer to North Asian populations than it is to any other populations, suggesting that it is more likely of North Asian origin. The results based on autosomal data do not support the hypothesis of Southeast Asian origin which was proposed by Tuner 2nd(1976)4. In addition, PCA revealed that two modern Japanese are located between mainland Asian populations and Jomon populations, consistent with the notion that they are the descendents of the admixture of mainland Asians and Jomons (Figure 3B). Furthermore, the clustering of Jomon populations inferred from Hondo and Ryukyuan Japanese suggested that their respective Jomon components were of similar, if not identical, origins (Figure 3A &B).

Figure 3: Genetic affinities between Jomon and other Asia populations.

Figure 3

A. NJ tree based on pairwise genetic distance. Each inferred Jomon population was named in population IDs of its admixed descendants and continental donors (JOMON ML-NH, JOMON ML-SH, JOMON ML-NHK, JOMON RK-NH, JOMON RK-SH and JOMON RK-NHK, respectively). B. Populations presented on a 3D plot with axis of PC1, 2 and 3 from PCA analysis. Features of the genetic affinities were the same as those were discovered by NJ tree.

Discussion

Through the estimations and inferences presented above, this study may shed light on the understanding of peopling of Japan. A few critical issues related to the findings of this work need to be further scrutinized.

Our result suggested D2 lineage of Y chromosome provides insufficient information on Jomon’s origin. Sharing of haplogroup D-M174 between central Asian populations and Japanese has been recognized as evidence of central Asian origin for paternal lineage of Paleolithic Japanese6. However, this study showed that some populations carrying branches of Y haplogroup D-M174 (D*: 10% in Dai; D1: 7.7% in Chuang, 2.59% in Tujia; D3: 28.89% in Naxi) showed little genetic relationship with the inferred Jomon populations (Figure 3)13. Furthermore, Y haplogroup D-M174 appears rarely in North Asian populations when the populations have a close genetic relationship with Jomon (Figure 3). The only appearance of D2 lineage in Japanese and the widespread geographic distribution of D-M174 made it practically impossible to pinpoint a population in the continent that provided the D2 lineage to Japanese. In contrast, autosomal markers indeed provide additional information that connects Jomon and North Asians.

In this study, a specified model was used to evaluate genetic admixture in modern Japanese populations. However, there is another powerful approach that was commonly applied in data analysis for population admixture, Bayesian method implemented in STRUCTURE. The Bayesian method focuses on a genetic inheritance model specified in terms of the proportion of an individual’s genome originating from each of a set of possible subpopulations21. The method is powerful and well recognized. However, when population history is partially understood and the divergence among ancestral populations is relatively small, performance of the Bayesian method is not fully clarified yet22. We applied the Bayesian method on 4 Japanese populations and 9 other East Asian populations with assumption that all the populations shared 2, 3, or 4 independent ancestry populations (Figure 4). None of inferred genetic components from STRUCTURE could well explain the great frequency difference of Japanese specific Y lineages, D2 and C1, between modern Hondo Japanese and Ryukyuans, while our estimations were concordant with the previous reports (Figure 2 & 3). The comparison suggested a specified model could be superior when population history was partially known.

Figure 4: Estimated admixtures with different pre-given value for number of genetic components in STRUCTURE 2.3.

Figure 4

Geographic distribution of lineages explained the great contribution of Yayoi in our results. Hammer et al. investigated geographic distribution of Y lineages in Japanese populations. Haplogroup frequencies of the Y lineages showed U-shape cline with significant correlation with geographic distance of the populations from Kyushu. In briefs, the frequency of D2 lineage increased with increase of the distance meanwhile frequencies of O lineages decreased6. The O lineages were recognized as a Yayoi founding lineage and D2 lineage was believed to be Jomon specific6,23. Therefore, the pattern of geographic distribution of lineages supported published archeological and anthropological results about population expansion during Jomon and Yayoi period in Japan. The archeological studies suggested general demographic density was significantly greater in eastern Japan compared to western Japan around the 3,300 years BP and a rapid increase first happened in West Japan around 2,000 years BP24. The studies of physical anthropology on human skeleton showed the new continental immigrants in West Japan, Yayoi people, have better capability to achieve enough foods to feed more people than Jomon24,25. The pattern of population expansion may explain the great genetic contribution (about 60–72%) of Yayoi in extent Japanese. Size of continental immigration was not necessary to be very large but descendants of the immigrants increased rapidly and subsequently dispersed from West Japan to other regions. Population admixture between the continental descendants (Yayoi) and Jomon descendants shaped genetic pattern of extent Japanese. Straits between Japanese islands and Asian mainland may not act as effective barriers to the genetic admixture.

This study supplied a genetic view for peopling of Japan. Both contributions and genetic affinity of Paleolithic Jomon were investigated in quantitative approach. However, the results should be improved continuously in further analysis. At first, the demographic model shall be improved when more data become available across Eurasia, especially from East Asia. Any improvement for the demographic model will lead to better estimation and inference in the model-based approach. The second, the used divergence time between historical Jomon and continental Yayoi should be validated with increased lines of evidence in future although both archaeological evidences and genetic studies supported a divergence time between Jomon and continental populations is properly around 20,000 years BP5,6. Furthermore, relatives of Yayoi in Asian mainland should be specified further.

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