Y Chromosomes of 40% Chinese Descend from Three Neolithic Super-Grandfathers

Here we present selected parts of the corresponding paper by Shi Yan, Chuan-Chao Wang, Hong-Xiang Zheng, Wei Wang, Zhen-Dong Qin, Lan-Hai Wei, Yi Wang, Xue-Dong Pan, Wen-Qing Fu, Yun-Gang He, Li-Jun Xiong, Wen-Fei Jin, Shi-Lin Li, Yu An, Hui Li, Li Jin.

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“Demographic change is one of the central questions in understanding human history, and strong population expansions may be linked to various events as climate changes, alteration of social structure, or technological innovations. The recent advent of next-generation sequencing technology enabled systematic analysis of the population history using the information from the whole genome with less ascertainment bias, so we can re-assess how the various factors have influenced the human population size and structure. Recent analyses of mitochondrial genomes revealed that the expansions of female lineages of East Asians and those of Europeans started before the Neolithic Era, contradictory to the hypothesis that the agricultural innovation constitutes the primary driving force of population expansions. These observations prompted this study to investigate expansions of male lineages.

The Y chromosome contains the longest non-recombining region in the human genome, making it an informative tool for reconstructing genetic relationship of human populations and paternal lineages, and dating important evolutionary and demographic events. However, the sequencing data of Y chromosomes of human populations were insufficient and biased even for those of current 1000-genome project for which coverage on Y chromosome was low.

According to the phylogenetic tree of Y chromosome, all the modern males could be categorized into 20 major monophyletic or paraphyletic groups (referred to as A to T) and their subclades. Nearly all the Y chromosomes outside Africa are derivative at the SNP M168 and belong to any of its three descendent super-haplogroups – DE, C, and F, strongly supporting the out-of-Africa theory. The time of the anatomically modern human’s exodus from Africa has yielded inconsistent results ranging from 39 kya, 44 kya, 59 kya, 68.5 kya to 57.0–74.6 kya.

To achieve sufficiently high coverage in the non-recombining regions of Y chromosome (NRY) and an adequate representation of individual samples, we selected 110 males, encompassing the haplogroups O, C, D, N, and Q which are common in East Eurasians, as well as haplogroups J, G, and R which are common in West Eurasians, and sequenced their non-repetitive segments of NRY using a pooling-and-capturing strategy.

The most surprising discovery in the tree is the three star-like expansions in Haplogroup O3-M324, i.e. under the M117 clade, the M134xM117 paragroup, and the 002611 clade. Here we denote the three star-like expansions as Oα, Oβ, and Oγ, respectively. Since the sample selection for high-throughput sequencing was intended for representing a wide variety of clades in East Asian populations, a star-like expansion indicates successful expansion of male lineages within a very short period (<500 years). These three clades are present with high frequency across many extant East Asian populations and encompass more than 40% of the present Han Chinese in total. It is conspicuous that roughly 300 million extant males are the patrilineal progenies of only three males in the late Neolithic Age.

The expansion dates are estimated 5.4 kya for Oα, 6.5 for Oβ, and 6.8 for Oγ, after the shift to intensive agriculture in North China (since 6.8 kya), in particular, during the Yangshao Culture (6.9–4.9 kya) in Central Yellow River Basin, Majiayao Culture (6.0–4.9 kya) in the Upper Yellow River Basin, and the Beixin (7.4–6.2 kya) – Dawenkou Culture (6.2–4.6 kya) in the Lower Yellow River Basin. We therefore propose that in the late Neolithic Age, the three rapidly expanding clans established the founding patrilineal spectrum of the predecessors in East Asia.

This study shows that all the strongly expanding Y chromosomal haplogroups (i.e. O-M175 or C-M130) had already migrated to East Asia more than 20 thousand years before their Neolithic expansion, thus supporting a boom of local farmers in China, which is consistent with the independent origin of agriculture.

The significant improvement of accuracy of dating in this study comparing to former East Asian studies is attributed to the large number of newly discovered SNPs. It is noted that the relative standard deviation of calculated divergence time is in inverse proportion to the square root of observed SNP occurrence.

Since all the Paleolithic divergences of Y chromosome lineages are binary, the three roughly contemporaneous star-like expansions revealed in this study indicate a remarkable demographic change in the late Neolithic Age. The earliest agriculture in North China emerged before 10 kya, however, no distinct Y chromosomal expansion could be related to this event. The three star-like expansions happened several thousand years later, thus are likely linked to middle Neolithic cultures such as Yangshao (6.9–4.9 kya) and Dawenkou Culture (6.2–4.6 kya) in the Yellow River Basin.

Although without ancient DNA proofs, we cannot yet confirm the initial expanding regions of these three clans, whether they were original in the middle or lower reach of Yellow River Valley or migrated from the vicinity, we are now at least certain that a majority of Han Chinese did derive from just a few patrilineal ancestors in the Neolithic Age. Whether each of them could be related to the legendary Emperors Yan and Huang or their tribes, is to be solved with more prudence and with the help of interdisciplinary genetic, archeological, ethnical, and documentary studies.

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(One may find the complete paper here: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0105691)

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