Genomic insights into the admixture history and adaptive evolution of the Zhuang people

The Zhuang, China's largest ethnic minority with over 17 million individuals, represent a critical yet understudied population for understanding East Asian genetic diversity and population history. Here, we present the first high-coverage whole-genome (>30×) and exome (>70×) sequencing study of the Zhuang (ZUN), integrating ancient and modern genomic data to reconstruct their evolutionary trajectory. We show that ZUN derive ∼68% of their ancestry from the Tai-Kadai-speaking people, diverging ∼3,000 to 5,000 years ago (ya), with the Maonan as their closest genetic relatives. Our analyses support a shared origin of Tai-Kadai and Austronesian populations ∼7,000 ya, predating their divergence from Sino-Tibetan groups ∼16,000 ya. Substantial gene flow from Han Chinese since ∼4,000 ya reduced genetic divergence between ZUN and northern East Asians to ∼12,000 years. The ZUN ancestral gene pool formed 5,000 to 3,000 ya through multiple admixture waves, with 87% contribution from southern populations and 12% from northern groups. Demographic modeling indicates continuous population expansion until ∼10,000 ya, followed by a pronounced growth surge over the past 400 years. Adaptive selection signatures highlight genes linked to immune response (IGH cluster), lipid metabolism (FADS1/2), wound healing (TMEM121), and environmental adaptation (ABCC11), suggesting dietary shifts and tropical pathogens as key evolutionary drivers. Furthermore, the ZUN genetic profile reflects their role as a regional hub for gene flow into neighboring populations, coinciding with Han migrations during the Qin dynasty. Together, these results identify the Zhuang as descendants of Baiyue populations with a distinctive dual ancestry shaped by Neolithic southern and northern East Asians.