Haplotype-Resolved Genome of Schizothorax nukiangensis Sheds Light on Polyploidy and Altitudinal Adaptation in Freshwater Fishes
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Chong Wang,
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Xuedie Gu,
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Guoliang Lin,
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Shuwei Liu,
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Guozheng Liao,
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Yuhui Du,
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Bangyang Sun,
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Tingchu Wei,
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Chengzhi Ding,
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Ya-Ping Zhang,
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Yan Li,
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Xiao-Yong Chen,
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Jing Luo
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Abstract
Polyploidy results in genome redundancy and drives ecological diversification in freshwater fishes, yet the genomic architecture and adaptive significance of recent polyploidization in high-altitude ecosystems remain poorly understood. Herein, after determining genome size and karyotype, we tackle the long-standing challenge of resolving highly similar homologous chromosomes in autopolyploid vertebrates. By integrating long-read sequencing, Hi-C scaffolding, and haplotype-specific phasing, we assemble a haplotype-resolved genome of the autotetraploid Schizothorax nukiangensis, comprising 100 chromosomes grouped into 25 homologous sets, with a genome size of 3.59 Gb in one cell. Evidences consistently support its autotetraploid origin, with a lineage-specific polyploidization event dated to ~0.68 Ma. Comparative genomics reveals substantial expansions of gene families in innate immunity, redox regulation, and transposon activity, suggesting genome remodeling might have contributed to adaptation in hypoxic, pathogen-rich, and fast-flowing mountain rivers. Population genomics across three elevational zones reveal subtle yet significant structure and identify candidate genes under selection related to skeletal development, immune defense, and ciliary function, consistent with adaptation to the torrents or rapids in fast-moving rivers characteristic of steep mountain ranges. Transcriptomic profiling further shows altitude-associated upregulation of genes related to immune responses and oxidative stress mitigation, which is consistent with other reported schizothoracines, highlighting convergent molecular strategies for altitude adaptation. Collectively, these demonstrate that recent autotetraploidization, coupled with gene family innovation and homeolog-specific expression divergence, has facilitated the ecological success of Sc. nukiangensis in extreme environments of the Salween River. This work provides important insights into the genomic imprints underlying adaptation in high-altitude freshwater vertebrates.
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