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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.
https://www.science.org/doi/10.1126/sciadv.abh2419
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.
An enduring hypothesis on the origin of modern Japanese populations proposes a dual-structure model (5), in which Japanese populations are the admixed descendants of the indigenous Jomon and later arrivals from the East Eurasian continent during the Yayoi period. This hypothesis was originally proposed on the basis of morphological data but has been widely tested and evaluated across disciplines [see a recent review in (6)]. Genetic studies have identified population stratifications within present-day Japanese populations, supporting at least two waves of migrations to the Japanese archipelago (7–10). Previous ancient DNA studies have also illustrated the genetic affinity of Jomon and Yayoi individuals to Japanese populations today (11–15). Still, the demographic origins and impact of the agricultural transition and later state formation phase are largely unknown. From a historical linguistic standpoint, the arrival of proto-Japonic language is theorized to map to the development of Yayoi culture and the spread of wet rice cultivation (6). However, archaeological contexts and their continental affiliations are distinct between the Yayoi and Kofun periods (1); whether the spread of knowledge and technology was accompanied by major genetic exchange remains elusive.
Here,we report 12 newly sequenced ancient Japanese genomes spanning 8000 years of the archipelago’s pre- and protohistory (Fig.1and Table1).To our knowledge, this is the largest set of time-stamped genomes from the archipelago, including the oldest Jomon individual and the first genomic data from the imperial Kofun period. We also include five published prehistoric Japanese genomes in our analysis: three Jomon individuals (F5 and F23 from the Late Jomon period and IK002 from the Final Jomon period) (12–14),as well as two 2000-year-old individuals associated with the Yayoi culture from the northwestern part of Kyushu Island, where skeletal remains exhibit Jomon-like characters rather than immigrant types but other archaeological materials clearly support their association with the Yayoi culture (15, 16).Despite this morphological assessment (16),these two Yayoi individuals show an increased genetic affinity to present-day Japanese populations compared with the Jomon, implying that admixture with continental groups was already advanced by the Late Yayoi period (15).Integrating these Japanese genomes with a larger ancient genomic dataset spanning the Central and Eastern Steppe (17, 18),Siberia (19),Southeast Asia (12),and East Asia (15, 20, 21),our study aims to better characterize the preagricultural populations of the Jomon period, as well as the subsequent migrations and admixtures that have shaped the genetic profile of the archipelagotoday.
Genetic distinction between different cultural periods
We explored the genetic diversity within our time series data by looking at the shared genetic drift between all pairwise comparisons of individuals from both the ancient and modern (SGDP) Japanese populations using the statistic f3(Individual_1, Individual_2; Mbuti) (Fig. 2A). Our results very clearly define three distinct clusters of Jomon, Yayoi, and Kofun individuals, the last of whom group with the modern Japanese individuals, suggesting that cultural shifts were accompanied by genomic changes. Despite the large spatial and temporal variation in the Jomon dataset, extremely high levels of shared drift are observed between all 12 individuals. The Yayoi individuals are most closely related to each other and also have a higher affinity to the Jomon than to the Kofun individuals. The Kofun and modern Japanese individuals are almost indistinguishable from one another by this metric, implying some level of genetic continuity over the past 1400 years.
https://www.science.org/doi/10.1126/sciadv.abh2419