Paleolithic Contingent in Modern Japanese: Estimation and Inference using Genome-wide Data

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.