Multiple founding paternal lineages inferred from the newly-developed 639-plex Y-SNP panel suggested the complex admixture and migration history of Chinese people

Abstract

Non-recombining regions of the Y-chromosome recorded the evolutionary traces of male human populations and are inherited haplotype-dependently and male-specifically. Recent whole Y-chromosome sequencing studies have identified previously unrecognized population divergence, expansion and admixture processes, which promotes a better understanding and application of the observed patterns of Y-chromosome genetic diversity. Here, we developed one highest-resolution Y-chromosome Single Nucleotide Polymorphisms (Y-SNP) panel targeted for uniparental genealogy reconstruction and paternal biogeographical ancestry inference, which included 639 phylogenetically informative SNPs (Y-SNPs). We genotyped these loci in 1033 Chinese male individuals from 33 ethnolinguistically diverse populations and identified 257 terminal Y-chromosomal lineages with frequency ranging from 0.010 (singleton) to 0.0687. We identified six dominant common founding lineages associated with different ethnolinguistic backgrounds, which included O2a2b1a1a1a1a1a1a1-M6539, O2a1b1a1a1a1a1a1-F17, O2a2b1a1a1a1a1b1a1b-MF15397, O2a2b2a1b1-A16609, O1b1a1a1a1b2a1a1-F2517, and O2a2b1a1a1a1a1a1-F155. The AMOVA and nucleotide diversity estimates revealed considerable differences and high genetic diversity among ethnolinguistically different populations. We constructed one representative phylogenetic tree among 33 studied populations based on the haplogroup frequency spectrum and sequence variations. Clustering patterns in principal component analysis and multidimensional scaling results showed a genetic differentiation between Tai-Kadai-speaking Li, Mongolic-speaking Mongolian, and other Sinitic-speaking Han Chinese populations. Phylogenetic topology inferred from the BEAST and Network relationships reconstructed from the popART further showed the founding lineages from culturally/linguistically diverse populations, such as C2a/C2b was dominant in Mongolian people and O1a/O1b was dominant in island Li people. We also identified many lineages shared by more than two ethnolinguistically different populations with a high proportion, suggesting their extensive admixture and migration history. Our findings indicated that our developed high-resolution Y-SNP panel included major dominant Y-lineages of Chinese populations from different ethnic groups and geographical regions, which can be used as the primary and powerful tool for forensic practice. We should emphasize the necessity and importance of whole-sequencing of more ethnolinguistically different populations, which can help identify more unrecognized population-specific variations for the final promotion of Y-chromosome-based forensic applications.

Paternal genomic resources from the YanHuang cohort suggested a Weakly-Differentiated Multi-source Admixture model for the formation of Han’s founding ancestral lineages

“…To explore the genetic affinity and admixture signature between the Han Chinese and other ethnolinguistic populations in East Asia, we aggregated our data with the published available haplogroup information, resulting in a comprehensive dataset encompassing 10,481 individuals from 54 ethnolinguistically diverse populations belonging to four language families (Lang et al 2019; Song et al 2019; Xie et al 2019; Wang et al 2021b; Wang et al 2021c; Song et al 2022; Wang et al 2022b; He et al 2023a). We performed PCA based on haplogroup frequency at the fourth level, aiming to elucidate the genetic relationship among the combined populations.…”

“…Moreover, with the comprehensive sampling coverage, Li et al unveiled the fine-scale matrilineal genetic divergence of the Han Chinese related to the river barriers and underscored the significant influence of agriculture technology innovation on shaping the matrilineal genetic variations (Li et al 2019b). Although the prior research on the paternal genetic architecture of the Han Chinese had been substantially conducted (Wen et al 2004a; Xue et al 2008; Lang et al 2019; He et al 2023a), the restricted number of Y-SNPs and/or limitation of sampling bias have hindered our understanding of the picture of fine-scale paternal population structure and the critical factors in shaping the paternal genetic landscape as the patrilocality and matrilocality residence models possess differentiated role in the human Y-chromosome genetic diversity and variation spectrum.…”