Evolutionary profiles and complex admixture landscape in East Asia: New insights from modern and ancient Y chromosome variation perspectives

Abstract

Human Y-chromosomes are characterized by nonrecombination and uniparental inheritance, carrying traces of human history evolution and admixture. Large-scale population-specific genomic sources based on advanced sequencing technologies have revolutionized our understanding of human Y chromosome diversity and its anthropological and forensic applications. Here, we reviewed and meta-analyzed the Y chromosome genetic diversity of modern and ancient people from China and summarized the patterns of founding lineages of spatiotemporally different populations associated with their origin, expansion, and admixture. We emphasized the strong association between our identified founding lineages and language-related human dispersal events correlated with the Sino-Tibetan, Altaic, and southern Chinese multiple-language families related to the Hmong-Mien, Tai-Kadai, Austronesian, and Austro-Asiatic languages. We subsequently summarize the recent advances in translational applications in forensic and anthropological science, including paternal biogeographical ancestry inference (PBGAI), surname investigation, and paternal history reconstruction. Whole-Y sequencing or high-resolution panels with high coverage of terminal Y chromosome lineages are essential for capturing the genomic diversity of ethnolinguistically diverse East Asians. Generally, we emphasized the importance of including more ethnolinguistically diverse, underrepresented modern and spatiotemporally different ancient East Asians in human genetic research for a comprehensive understanding of the paternal genetic landscape of East Asians with a detailed time series and for the reconstruction of a reference database in the PBGAI, even including new technology innovations of Telomere-to-Telomere (T2T) for new genetic variation discovery.

Keywords: Ancient DNA; East Asian; Evolutionary history; Founding lineage; Genomic resources; Y-chromosome genetic diversity.

Fig. 1

The timeline of different human genome projects, sequencing techniques, platforms and forensic applications. Since our focus is on developing forensic Y-SNP panels, the other events are only partially presented. The abbreviations are presented as follows. HGP: Human Genome Project. Hapmap: Haplotype Map. SGDP: Simons Genome Diversity Project. GSRD-100K^WCH: Genome Sequence of Rare Disease-100k^{West China}. GAsP: GenomeAsia 100K Project. ChinaMAP: China Metabolic Analytics Project. HGDP: Human Genome Diversity Project. T2T: Telomere-to-Telomere. WBBC: Westlake BioBank for Chinese. 10K-CPGDP: 10K Chinese Person Genomic Diversity Project.

Fig. 2

The simplified Y-chromosome phylogenetic tree. The haplogroups that appear in the review are shown in the tree. The topology structure and nomenclature are compatible with the International Society of Genetic Genealogy (ISOGG) Y-DNA Haplogroup Tree 2019–2020 version 15.73 (http://www.isogg.org/tree/). * indicates that the haplogroup was present in previous literature but was not included in the ISOGG.

Fig. 3

Distribution patterns of Y chromosome haplogroups in modern populations. (A) The phylogeography of haplogroups in East Asia. In China, we calculate haplogroup frequency by province. (B) The distribution patterns of haplogroups in different ethnolinguistic populations. The detailed information is presented in Table S1.

Fig. 4

Distribution patterns of East Asian-dominant haplogroups in spatiotemporally different populations inferred from ancient DNA over time. (A) Patterns of the Y chromosome lineages inferred from ancient DNA extracted 5300 years ago. (B) Patterns of the Y chromosome lineages inferred from ancient DNA ranging from 5300 to 3000 years BP. (C) Patterns of the Y chromosome lineages inferred from ancient DNA from 3000–2000 years BP. (D) Patterns of the Y chromosome lineages inferred from ancient DNA from 2000 years BP. Due to the overlap of the Xinjiang and Mongolia sites, we show the overlap of the sites in the upper left corner of each figure. The detailed information is shown in Table S2.