Population dynamics in the Japanese Archipelago since the Pleistocene

doi:10.21203/rs.3.rs-145519/v1

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Population dynamics in the Japanese Archipelago since the Pleistocene

https://doi.org/10.21203/rs.3.rs-145519/v1

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published 12 Jun, 2021

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The Japanese Archipelago is widely covered with acidic soil made of volcanic ash, an environment which is detrimental to the preservation of ancient biomolecules. More than 10,000 Palaeolithic and Neolithic sites have been discovered nationwide, but few skeletal remains exist and preservation of DNA is poor. Despite these challenging circumstances, we succeeded in obtaining a complete mitogenome sequence from Palaeolithic human remains. We also obtained those of Neolithic (hunting-gathering Jomon and the farming Yayoi cultures) remains, and over 2,000 present-day Japanese. The Palaeolithic mitogenome is potentially an ancestral type of haplogroup M, suggesting it is not only connected to present-day Japanese but also present-day East Asians. There were no changes in the gene pool from the hunting-gathering (Jomon) to the farming cultures (Yayoi), and this is different from in Europe, where there was no genetic continuity between hunter-gatherers and farmers. We also found that a vast increase of population size happened and has continued since the Yayoi period, characterized with paddy rice farming. It means that the cultural transition, i.e. rice agriculture, had significant impact on the demographic history of Japanese population.

Anthropology

Evolutionary Genetics

population dynamics

Japanese Archipelago

Pleistocene

The Japanese Archipelago located in the boundary of the Eurasian, the North American, the Pacific and the Philippine Sea Plates was created by separating from the Asian continent by 15 million years ago. Archaeological evidence indicates the first appearance of people in the Japanese Archipelago during the late Pleistocene between 40,000 and 30,000 years ago. The prehistoric era after the Palaeolithic era is typically split into two contrasting periods, Jomon and Yayoi [1]. The Jomon period is characterized by hunter-gatherer subsistence that persisted for more 10,000 years [2, 3]. On the other hand, the Yayoi period saw a sudden rise in paddy rice farming [1] and it is thought that this style of rice production was introduced into the Japanese Archipelago by immigrants from mainland Asia [4]. The Japanese Archipelago is widely covered with acidic soil made of volcanic ash, making ancient DNA studies challenging. Here we investigate the population dynamics in the Japanese Archipelago using complete mitogenome sequences from the Palaeolithic, Jomon, and Yayoi periods, and find no drastic substitutions in gene pool among them, unlike that observed in Europe [5–10]. Instead, through demographic analysis using over 2,000 present-day Japanese, we observe drastic population explosion across cultural transition from hunter gathering to farming.

Anatomically modern Homo sapiens left Africa and spread throughout Europe and Asia around 50,000 years ago, during the Last Glacial Period (LGP) (70,000–10,000 BP). This was a period in which the environment is known to have undergone short, rapid fluctuations in temperature. During the transition from the LGP to the present Holocene, there was also a temporary return to glacial conditions, known as the Younger Dryas. This rapid climate change has been shown to be strongly associated with the widespread extinction of megafauna [11, 12]. Analysis of mitochondrial DNA from archaeological human remains dating to the Late Pleistocene has identified individuals belonging to haplogroup M that populated Europe before the LGP. M is a haplogroup that is frequently observed in present-day Asian populations but is not found in present-day European populations, and changes in the European gene pool during the LGP suggest that a genetic bottleneck or turnover occurred [8, 9]. However, whether a similar event occurred across East Asia is not clear. In addition, it has been shown that there was no genetic continuity between European hunter gatherers and farmers. In other words, hunter-gatherer groups were replaced by agriculture-based groups [5–7, 10].

Mitogenome of the Palaeolithic remains

We successfully determined a highly accurate complete mitochondrial genome sequence of 20,000-year-old Minatogawa 1 (Minato1), a plausible direct descendant of the initial Out-of-Eurasia into the Japanese Archipelago (Fig. 1, Table 1 and Supplementary Table S1). Its sequence obtained with average depth of 52 was classified into haplogroup M, and carries no substitutions that are defining subgroups of haplogroup M. Figure 2 shows a Bayesian phylogenetic tree of mitogenome of 18 ancient and 171 present-day individuals in the Japanese Archipelago. Figure 3 shows a Mutli Dimensional Scaling (MDS) plot of mitogenome of 1 Palaeolithic, 13 Jomon, 4 Yayoi, and 2,062 present-day individuals in the Japanese Archipelago. Minato1 has the potentially ancestral type of haplogroup M, which can be seen neither in 2,062 present-day Japanese samples newly obtained in this study nor in 21,668 present-day Han Chinese samples recently published [13]. Haplogroup M is found at high frequency in present-day Asians, Australasians, and indigenous Americans. The fact that Minato1 carried a mitochondrial genome that is potentially ancestral type of haplogroup M suggests (a) there is at least some population continuity from the late Pleistocene to present-day human populations in the Japanese Archipelago and (b) Minato1 is not only connected to present-day Japanese but also present-day East Asians. A 40,000-year-old Tianyuan individual, excavated from northern China, was reported to be the mitochondrial sequence of ancestral-type haplotype B having four singletons (private mutations), i.e. a common ancestor of present-day mitogenome belonging to haplogroup B. Afterwards it is shown that the Tianyuan individual is not from a population that is directly ancestral to any present-day East or Southeast Asians, but rather belonged to a population that diverged from the population that contributed to present-day East and Southeast Asians [14,15]. Due to fluctuating global warming, Palaeolithic period from the LGP is supposed to be a difficult time to survive in [11,12], and changes in the gene pool are expected to occur various populations all across the world. However, the results of phylogenetic network including Minato1 and Tianyuan individuals show that changes in gene pool during the LGP had not occurred in East Asia, in contrast with in Europe.

Mitogenome of the hunting-gathering Jomon remains

We further successfully determined highly accurate complete mitochondrial genome sequences with average depths of coverage from 11 to 5,891 using 8,300- to 2,300-year-old Jomon individuals (10 individuals from six archaeological sites, Fig. 1, Table 1 and Supplementary Table S1). All of the Jomon individuals fall into the same clusters with present-day Japanese in phylogenetic network, Bayesian phylogenetic tree and Mutli Dimensional Scaling (MDS) plot (Figs. 2 and 3). This shows population continuity from Jomon period to present-day in the Japanese Archipelago, meaning no dynamic change in the gene pool of people living in the Japanese Archipelago from the Palaeolithic to Neolithic periods, unlike in West Eurasia. The results obtained also show that most of the Jomon individuals in our collection examined are of haplogroups M or N, and many of them are of sub-haplogroups M7a or N9b in the narrow taxonomic group (Table 1 and Supplementary Table S1). This is consistent with the previous observations from PCR-based typing [16,17]. Both haplogroups M7a and N9b characteristic of Jomon individuals have been inherited by the present-day Japanese individuals; 7.9% and 1.3% among the present-day Japanese population, respectively (Supplementary Table S2).

Mitogenome of the farming Yayoi remains

In addition, we too successfully determined highly accurate complete mitochondrial genome sequences of four individuals from Yayoi period with average depths of coverage from 13 to 5891 (each two individuals from the Hanaura and Doigahama Yayoi sites, respectively. Fig. 1, Table 1 and Supplementary Table S1). The Yayoi period started by the life style of paddy rice farming that was brought into Japanese Archipelago by the Out-of-Eurasians. The results show that three of the Yayoi individuals belong to haplogroup D4 (Table 1). D4 is the most common haplogroup in present-day Japanese (34.3%) (Supplementary Table S2), which is also common throughout East Asia [13,18]. Like the Jomon individuals, all of the Yayoi individual fall into any of the clusters of the phylogenetic network, MDS and Bayesian phylogenetic tree that are constructed together with the present-day Japanese people, although the Jomon and Yayoi people have some mitochondrial sub-haplogroups characteristic to each of them (Figs. 2 and 3).

Estimating past demographic trends

Figures 4 shows the phylogenetic network and the Neighbor-Joining phylogenetic tree for 324 world-wide ancient and present-day individuals belonging to macrohaplogroup M (including C, D, G, M7, M8, M10, and Z), and macrohaplogroup N (including A, B, B5, F, N9, R9, R11, and Y), respectively. The gene pool of the present-day Japanese has been established, swallowing all of the genetic diversities of the people living in the Japanese Archipelago during more than 10,000 years, starting from the Palaeolithic period through the hunter-gatherer Jomon period, farming Yayoi period, and so on. These observations can suggest that there was no conflict between indigenous Jomon hunter-gatherers and migrating Yayoi farmers. This intercultural fusion from genetic points of view is quite different from observations in Europe [5-7,10].

Bayesian-Skyline Plot (BSP) analysis using 2,062 present-day Japanese found three large population increases, at 45,000-35,000 BP, 15,000-12,000 BP, and 3,000 BP (Fig. 5). These correspond with a rise in temperatures seen in the Late Pleistocene, the dawn of agriculture in East Asia, and the beginning of the Yayoi period, respectively. In a recent study relating to East Asia, demographic simulations were undertaken using complete mitochondrial DNA sequences from 21,668 present-day Han Chinese individuals [13]. The results showed that there was a population increase towards the end of the LGP around 45,000-35,000 BP, followed by another, more rapid increase during the Neolithic period 15,000-12,000 BP. The first two population increases seen in the present-day Japanese populations should have taken place before their ancestors migrated to the Japanese Archipelago, suggesting that these increases took place before Out-of-Eurasia. However, the population increase corresponding to the beginning of the Yayoi period was not observed on the mainland Han Chinese populations, and thus was considered to be a phenomenon unique to the Japanese Archipelago, namely that caused by the Out-of-Eurasians after the Yayoi period. It is easily expected that the Yayoi migrant bringing rice paddy farming should have a significant impact on the number of population and population structure in the Japanese Archipelago. And further population increase afterwards could be related to the introduction of ironware into the Japanese Archipelago, which allowed for more efficient rice paddy farming and a more stable food supply [19]. Given all the findings obtained, our results show that genetic makeup of the present-day Japanese populations is built after migrant Yayoi farmers coming over from the Asian mainland. But we cannot ignore contribution of the Jomon people to the present-day Japanese population structure.

This paper is the first genome paper that disclosed population dynamics since the initial Out-of-Eurasians into in the Japanese Archipelago in the Palaeolithic period, through the hunting-gathering Jomon and the farming Yayoi periods, until the present-day. We have determined the first complete mitochondrial genome sequences dating to the Palaeolithic period in the Japanese archipelago. Minato1 individual has skeletal characteristics that are different from those of the Jomon people and the present-day Japanese people, highlighting the necessity of further research on the relationship between Palaeolithic people and Jomon people from both morphological and genetic perspectives. We show (a) there were no drastic substitutions in the gene pool since the initial wave of Out-of-Eurasia into the Japanese Archipelago of Palaeolithic period, (b) ancestors of the present-day Japanese had experienced three large population increases, but the first two of them before Out-of-Eurasia into the Japanese Archipelago. The third increase was a sharp one occurred in relatively short period, (c) gene pool of the Jomon hunter-gatherers has survived, even after migration of the Yayoi farmers and its subsequent population explosion. The following key questions remains open such as whether the migrating Yayoi farmers genetically mixed with the indigenous Jomon hunter-gatherers at each stage after the Yayoi migration (and, if so, how type of mix occurred) and whether population transformation across cultural transitions observed in Europe was worldwide versus local phenomena [20-22]. Anthropological evidence indicates the presence of convivial society among Jomon and Yayoi peoples. Ancient Japanese Archipelago should be an ideal field to elucidate interaction between hunter-gatherers and farmers and its accompanying population structure transformations.

Ancient samples

Bones and teeth from human remain representing 15 individuals (Table 1) from nine archaeological sites were sampled for ancient genome analyses; Minatogawa fissure and Mabuni hantabaru (Okinawa Pref.), Iyai rock-shelter (Gunma Pref.), Higasimyou and Hanaura (Saga Pref.), Todoroki shell midden (Kumamoto Pref.), Kasori shell midden and Ubayama shell midden (Chiba Pref.), Doigahama (Yamaguchi Pref.). Dates of five samples are available, the others are referenced on pottery typological chronology. Minato1 indicates many archaic morphological features, such as a thick and inferiorly wide skull vault, a small frontal bone with extremely developed temporal fossae, and a rugged facial profile. It is reasonable to suppose that it was remnants of the earliest Homo sapiens in East Asia, who somehow migrated to Okinawa Islands around 30,000 or 40,000 years ago and survived at least until around 20,000 years ago, keeping these archaic features [23,24].

Approval for the present study was provided by the Ethics Committee of Toho University School of Medicine (A18099_A18056).

DNA extraction, NGS library preparation, enrichment of the ancient mitochondrial genome and sequencing

DNA was extracted from bones and teeth, and NGS library was constructed according to our previous methods [25] with slight modifications as follows [26]. After exhaustively brushing to eliminate dirt and exogenous contaminants, the outer bone surface was mechanically removed with a sanding machine (Dremel) to further remove surface contaminants. The clean bone was cut into small pieces of approximately 1–2 cm³ using an electric drill cutter (Dremel). The bone fragments were cooled with liquid nitrogen, and fine powdered bone was obtained by grinding bone fragments in a mill (Multi-beads Shocker MB601U, YASUI KIKAI). During all steps of DNA extraction, NGS library preparation, and enrichment, we took all possible precautions to guard against contamination. Experiments were performed in a laboratory that is exclusively dedicated to ancient DNA work and is physically isolated from other molecular work laboratories. All manipulations were performed in a laminar flow cabinet routinely irradiated with UV light. Frequent surface cleaning was routinely performed before and after working. A facemask, head cap, and clean laboratory coat were always worn, and gloves were frequently replaced. All the procedures were conducted using new sterilized disposable tubes and filter pipette tips. All non-disposable glass and metallic materials were dry-heat sterilized at 160˚C for 2–4 hours. The powdered samples (10 to 200 mg) were digested in 0.5M EDTA (pH 8.0) for 2 h at 56 °C in a rotating hybridization oven, and the supernatant was removed by centrifugation. This decalcification step was repeated three times in total. DNA was extracted with phenol:chloroform:isoamyl alcohol (25:24:1), followed by extraction with an equal volume of chloroform. After centrifugation, the aqueous solution was removed and subsequently concentrated by centrifugation dialysis using an Amicon Ultra-15 30 kDa centrifugal filter (Merck Millipore) to a final volume of 200 μL. The DNA solution was purified with silica-based MiniElute spin columns (Qiagen) according to manufacturer's protocol. The obtained DNA was quantified using Quant-iT dsDNA HS assay kit (Thermo Fisher Scientific). Using the obtained DNA, we prepared single- or double-strand NGS libraries. For some samples, PreCR Repair Mix (New England BioLabs) treatment was done. Libraries were enriched for human mitochondrial genomes, using in-solution target enrichment (SureSelect, Agilent Technologies). The libraries were pooled sequenced on illumina MiSeq or HiSeq platform 1500 according to the manufacturer's instructions.

NGS data processing and ancient DNA authentication

Raw sequencing reads were trimmed by removing adapter sequences and low-complexity sequences with fastp ver. 0.20.0 [27]. The trimmed reads were mapped against the human mitogenome reference sequence rCRS [28], using the Burrows-Wheeler Alignment tool (BWA) [29] with optimal parameters for ancient DNA [30]. Reads with a mapping quality lower than 30 were filtered out and high-quality mapped reads were retained using samtools ver. 1.9 [31]. To minimize the effects of nucleotide mis-incorporations on building a consensus mitogenome sequence, the first two bases on each end of the read were clipped with BamUtil ver. 1.0.14 [32] according to our previous bioinformatics procedure [33]. Then, reads with a significant hit (E-value <= 1e-15) to non-human genomes (e.g., fungal or bacterial genomes) were identified by BLASTN and then were also filtered out. In addition, reads mapped to human nuclear genome sequences of hg19 were also removed as numts (nuclear copies of mitogenome). Finally, consensus sequences were built using MitoSuite [34], and their mitogenome haplogroup assignments were called with HaploGrep2 [35]. We checked variants using IGV software [36] based on PhyloTree Build 17 (http://www.phylotree.org/) [37]. To assess whether the results could be affected by present-day human contamination, sequences with ancient DNA specific cytosine to thymine substitutions (C to T) at the 5’ or 3’ molecule end were selected and analysed separately (supplementary Material online). DNA contamination was estimated using MitoSuite ver.1.0.9 [34].

Present-day Japanese samples

Present-day Japanese examined in this study are participants of the baseline survey in the Nagahama Study. The Nagahama Study is an ongoing community-based cohort study conducted by the Kyoto University Graduate School of Medicine and Nagahama City. The participants are members of the general population living in Nagahama City, a rural city of 125,000 inhabitants in Shiga Prefecture located in central Japan, aged 30 to 74 years old. The Ethics Committee of Kyoto University Graduate School and Faculty of Medicine (G0751-4), the Ethical Review Board of the Nagahama Study, and the Nagahama Municipal Review Board of Personal Information Protection approved all study procedures. Approval was also provided by the Ethics Committee of Department of Evolutionary Studies of Biosystems, SOKENDAI; The Graduate University for Advanced Studies (SKD2019HG001).

NGS data processing of present-day Japanese mitogenome DNA

Whole genome sequencing was conducted using the Illumina HiSeq X Ten sequencer (Illumina Inc., San Diego, CA, USA). After aligning the sequence reads onto the reference genome (GRCh37/hg19) using the Burrows-Wheeler Aligner [29] with default parameters, duplicate reads were marked using Picard. A total of 2,062 subjects were included in the present study, of which complete mitogenome sequences are available with high depth of coverage. Finally, consensus sequences were built from the BAM files of chrM using MitoSuite [34], and their mitogenome haplogroup assignments were called with HaploGrep2 [35]. (Supplementary Table S2). We checked variants using IGV software [36] based on PhyloTree Build 17 [37].

Statistical phylogenetic analyses

To produce Bayesian phylogenetic tree, we used mrbayes v. 3.2 [38]. “GTR + I + Γ” model was used for substitution model. Model was selected by Maximum Likelihood fits function in MEGA X [39]. We set the Markov Chain Monte Carlo (MCMC) chain length to 3.0 × 10⁶ with 7.5 × 10⁵ burn-in steps to collect sufficient samples for estimation. In this Bayesian tree, we selected 171 present-day Japanese mitochondrial genome sequences to cover major haplotypes belonging macro haplogroups M and N (see Supplementary Table S3 for the list of sequence used) and for the ease of computation. Our newly determined 15 ancient mitochondrial genome sequences were aligned together and included in the tree estimation. The tree was estimated by using haplogroup L0a (accession number: EF184601.1) as an outgroup. For MDS, we used 2,062 complete mitogenome sequences from Japanese population, which were produced in this study. Sequences without “N” nucleotide were used. We used mafft v7.471 to align these 2,062 sequences with rCRS sequence [40]. Mutations were scored relative to the rCRS and we extracted the coding regions. The 15 ancient mitochondrial genome sequences produced in this study were added to this multiple sequence alignment. MDS was performed on R software with cmdscale() function [41]. We used p-distance based on the number of differences on nucleotide sequences for MDS. We used MEGAX for obtaining p-distances [39]. A median-joining Network [42] was constructed by using PopART v1.7 [43] with a parameter “epsilon = 0”. We selected 287 modern Asian mitochondrial genome sequences to cover major haplotypes belonging macro haplogroups M and N. Also, 22 ancient mitochondrial genomes available were obtained. Together with above dataset, our newly determined 15 ancient mitogenome sequences were aligned, and then, variant sites in coding region of mitochondria genome was used as an input for the network analysis (see Supplementary Tables S3 and S4 for the lists of sequence used). The resultant network was manually modified to improve visibility on PopART.

Bayesian Skyline Plot (BSP)

To obtain BSP, we used BEAST v2.5.0 suite [44]. We applied the General time reversible model mutation model using gamma-distributed rate. A clock model was used assuming a log-normal distribution. We set the Markov Chain Monte Carlo (MCMC) chain length to 1 × 10¹⁰ with 1 × 10⁹ burn-in steps to collect sufficient samples for parameter estimation. We performed the MCMC simulation twice independently to confirm that the simulation converged to the same state. The time was scaled by the number of mutations for BSP construction. To estimate time in year, we assumed a molecular clock of 2.77 x 10^-8 [9] and applied the correction method of Soares et al. (2009) [45]. To scale the effective population size (Ne), we assumed a generation time of 25 years. The simulation results were analysed using Tracer v1.7.1 (http://tree.bio.ed.ac.uk/ software/tracer/).

Data availability

Sequencing data produced in this study have been deposited in the GenBank (accession no. LC521960- LC521962, LC597326-597337) and Human Genetic Variation Database (accession no. HGV0000011, http://www.hgvd.genome.med.kyoto-u.ac.jp) for ancient samples and present-day Japanese, respectively.

Acknowledgements

We would like to thank Koji Ishiya for processing and curating of NGS data, Masaki Fujita for valuable discussions, Katherine Hampson for English expressions, Koichi Matsuo for bone anatomy, Oki Nakamura and Kousaku Matsumoto for drawing Figure 1. We also thank Aiko Saso and Gen Suwa for access to the samples, Hideaki Kanzawa-Kiriyama for data of Funadomari, Hiroki Ota and Takashi Gakuhari for data of Ikawazu. This work was supported by Grant-in-Aid for JSPS KAKENHI Grant Number 17K07588, 19H05737, 20H01376, 20K15884 (to F.M.), 18H05511 (to J.G.), 17K07255 (to K.H.), and 17H00939 (to S.U.).

Author contributions

F.Mi. J.G. M.K. L.W., K.K., and S.U. designed this study and performed research. H.B., Y.T., O.K., M.M., and T.M. provided ancient samples and assembled archaeological and anthropological information. F.Mi. M.H., L.W., K.K., and S.U. performed ancient laboratory work. F.Ma. and K.H. provided present-day Japanese data and analyses genetic data. F.Mi., J.G., M.K., H.B., K.H., and S.U. wrote the manuscript. All authors reviewed the manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Supplementary Material The online version contains supplementary material available at https://.

Correspondence and requests for materials should be addressed to F.Mi. or J.G. or L.W.

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Population dynamics in the Japanese Archipelago since the Pleistocene

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