doi: 10.1126/sciadv.abh2419. Epub 2021 Sep 17.
Ancient genomics reveals tripartite origins of Japanese populations
Niall P Cooke 1, Valeria Mattiangeli 2, Lara M Cassidy 2, Kenji Okazaki 3, Caroline A Stokes 2, Shin Onbe 4, Satoshi Hatakeyama 5, Kenichi Machida 6, Kenji Kasai 7, Naoto Tomioka 8, Akihiko Matsumoto 9, Masafumi Ito 10, Yoshitaka Kojima 11, Daniel G Bradley 2, Takashi Gakuhari 11, Shigeki Nakagome 1 11
Affiliations
- PMID:34533991
- PMCID: PMC8448447
- DOI: 10.1126/sciadv.abh2419
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Ancient genomics reveals tripartite origins of Japanese populations
Niall P Cooke et al. Sci Adv..
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Abstract
Prehistoric Japan underwent rapid transformations in the past 3000 years, first from foraging to wet rice farming and then to state formation. A long-standing hypothesis posits that mainland Japanese populations derive dual ancestry from indigenous Jomon hunter-gatherer-fishers and succeeding Yayoi farmers. However, the genomic impact of agricultural migration and subsequent sociocultural changes remains unclear. We report 12 ancient Japanese genomes from pre- and postfarming periods. Our analysis finds that the Jomon maintained a small effective population size of ~1000 over several millennia, with a deep divergence from continental populations dated to 20,000 to 15,000 years ago, a period that saw the insularization of Japan through rising sea levels. Rice cultivation was introduced by people with Northeast Asian ancestry. Unexpectedly, we identify a later influx of East Asian ancestry during the imperial Kofun period. These three ancestral components continue to characterize present-day populations, supporting a tripartite model of Japanese genomic origins.
Figures
(A) Archaeological sites are marked with circles for individual genomes newly sequenced in this study and triangles if previously reported (see Table 1 and table S1). The colors represent three different periods of Japanese pre- and protohistory: Jomon, Yayoi, and Kofun. (B) Each individual is plotted with whole-genome coverage on thex axis and median age (years before present) on they axis. The nine Jomon individuals are split into five different subperiods on the basis of their ages (see note S1): Initial (JpKa6904), Early (JpOd274, JpOd6, JpOd282, JpOd181, and JpFu1), Middle (JpKo2), Late (JpKo13, JpHi01, F23, and F5), and Final (IK002).
(A) A heatmap of pairwise outgroupf3 statistic comparisons between all ancient and modern Japanese individuals. (B) Principal components analysis (PCA) visualizing ancient Japanese individuals (i.e., Jomon, Yayoi, and Kofun) and continental ancient individuals (presented as colored symbols) projected onto 112 present-day East Eurasians (gray circles with Japanese highlighted in dark green). (C) Selected individuals from an ADMIXTURE analysis (K = 11; complete pictures fromK = 2 toK = 12 are presented in figs. S5 and S6), showing a distinct Jomon ancestral component (represented by red), a component common in ancient samples from the Baikal region and the Amur River basin (represented by light blue) and a broad East Asian component (represented by yellow). A gray component that is most dominant in the Central Steppe is absent in the ancient and modern Japanese samples. The middle and bottom rows show selected Ancient East Eurasian populations from each geographical regions: Southern China (from left to right: Liangdao1, Liangdao2, and Xitoucun), Yellow River (YR) (Middle Neolithic, YR_MN; Late Neolithic, YR_LN; Late Neolithic, Upper_YR_LN; Late Bronze Age/Iron Age, YR_LBIA; and Iron Age, Upper_YR_IA), Northern China (Yumin, Bianbian, Boshan, and Xiaogao), West Liao River (WLR) (Middle Neolithic, WLR_MN; Late Neolithic, WLR_LN; Bronze Age, WLR_BA; Middle Neolithic individual from Haminmangha, HMMH_MN; and Bronze Age individual with a different genetic background from WLR_BA and WLR_BA_o), Amur River (AR) (Early Neolithic, AR_EN; and Iron Age, AR_IA and AR_Xianbei_IA), Baikal (Early Neolithic, Shamanka_EN and Lokomotiv_EN), and Central Steppe (Botai, CentralSteppe_EMBA, and Okunevo_EMBA).
(A) Maximum likelihood phylogenetic tree reconstructed by TreeMix under a model of two migrations. The tree shows a phylogenetic relationship among ancient (bold) and present-day (italic) populations. Colored arrows represent the migration pathways. The migration weight represents the fraction of ancestry derived from the migration edge. All other migration models fromm = 0 tom = 5 are presented in fig. S7. (B) ROH spectra for Mesolithic and Neolithic hunter-gatherers including the 8.8-ka-old JpKa6904. Total length of ROH is plotted against different sizes of homozygous fragments ranging from 0.5 to 100 Mb. (C) Fitting of the models under different combinations ofN (x axis) andT (y axis) for the 8.8-ka-old Jomon individual. Each point in the balloon plot represents a log10-scaled approximate Bayes factor (aBF) that compares likelihoods between a model with the highest likelihood and each of the other given models; the point with aBF = 0 is the model with the highest likelihood (N = 1000 andT = 20 ka ago; see fig. S10). NA means that aBF is not measurable for the model due to its likelihood equal to zero. (D) A comparison of outgroupf3 statistic results for the Jomon dataset divided into three subperiods measured usingf3(Jomon_Sub-Period,X; Mbuti) (see fig. S12 for an expanded analysis). The three subperiods are as follows: Initial Jomon (JpKa6906); Early Jomon (JpFu1, JpOd6, JpOd181, JpOd274, and JpOd282); and a merged group for all Middle, Late, and Final Jomon (F5, F23, IK002, JpHi01, JpKo2, and JpKo13).
(A) Geographical map highlighting results fromf4(Mbuti,X; Jomon, Yayoi); continental ancient populations who are significantly closer to the Yayoi than the Jomon (withZ > 3.0) are represented by red triangles, while those who are symmetrically related to the both populations are represented by gray circles. (B) Genetic ancestry of the Yayoi modeled with a two-way admixture of the Jomon and the other source represented by: Bronze Age or Middle Neolithic individuals from West Liao River (WLR_BA_o or HMMH_MN) or Baikal hunter-gatherer (Lokomotiv_EN). Vertical bars represent ±1 SE estimated by qpAdm. The values of admixture proportions are shown in table S7. (C) Correlation of shared genetic drift between the Yayoi and a Jomon individual with the geographic locations of Jomon sites. The spherical distance from the Yayoi site is measured with the Haversine formula (93). The map marks the archaeological site of Yayoi with a red arrow and the sites of Jomon by circles with different colors.
(A) Geographical maps highlighting results fromf4(Mbuti,X; Yayoi, Kofun); continental ancient and present-day populations who are significantly closer to the Kofun than the Yayoi with aZ score of >3.0 are represented by red triangles, while those that are symmetrically related to both populations are represented by gray circles. The populations tested are split into four different periods, depending on their ages: Upper-Paleolithic (>16,000 years B.P.), Jomon (from 16,000 to 3000 years B.P.), Post-Jomon (from 3000 years B.P. to the present), and present day. Han is highlighted by a blue triangle in the present-day panel. (B) Genetic ancestry of the Kofun individuals modeled with a three-way admixture of the Jomon, Northeast Asia (WLR_BA_o and HMMH_MN), and Han. Vertical bars represent ±1 SE estimated by qpAdm. The values of admixture proportions are shown in table S10.
The Jomon had a very unique genetic profile due to strong genetic drift and a long-term isolation in the Japanese archipelago. The rice cultivation was brought by the people who had Northeast Asian ancestry (represented by WLR_BA_o and HMMH_MN) in the Yayoi period. An additional wave of migration brought widespread East Asian ancestry (represented by Han) to the archipelago in the Kofun period. Since then, this tripartite ancestry structure has been maintained in the archipelago and become the genetic foundation of modern Japanese.
References
- K. Mizoguchi,The Archaeology of Japan: From the Earliest Rice Farming Villages to the Rise of the State (Cambridge Univ. Press, 2013).
- J. Habu,Ancient Jomon of Japan (Cambridge Univ. Press, 2004).
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