Chromosome-level genome assembly and population genomic analysis provide insights into the genetic diversity and adaption of Schizopygopsis younghusbandi on the Tibetan Plateau

Chaowei ZHOU , Yan ZHOU , Luohao XU , Fei LIU , Luo LEI , He GAO , Junting LI , Suxing FU , Yuting DUAN , Yougang TAN , Weihua MAO , Qiming WANG , Rongzhu ZHOU , Shijun XIAO , Chuan LIU , Haiping LIU

Integrative Zoology ›› 2025, Vol. 20 ›› Issue (6) : 1246 -1264.

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Integrative Zoology ›› 2025, Vol. 20 ›› Issue (6) :1246 -1264. DOI: 10.1111/1749-4877.12910
ORIGINAL ARTICLE
Chromosome-level genome assembly and population genomic analysis provide insights into the genetic diversity and adaption of Schizopygopsis younghusbandi on the Tibetan Plateau
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Abstract

The Yarlung Tsangpo River on the Tibetan Plateau provides a unique natural environment for studying fish evolution and ecology. However, the genomes and genetic diversity of plateau fish species have been rarely reported. Schizopygopsis younghusbandi, a highly specialized Schizothoracine species and economically important fish inhabiting the Yarlung Tsangpo River, is threatened by overfishing and biological invasion. Herein, we generated a chromosome-level genome of S. younghusbandi and whole-genome resequencing data for 59 individuals from six locations of the river. The results showed that the divergence time between S. younghusbandi and other primitive Schizothoracine species was ∼4.2 Mya, coinciding with the major phase of the Neogene Tibetan uplift. The expanded gene families enriched in DNA integration and replication, ion binding and transport, energy storage, and metabolism likely contribute to the adaption of this species. The S. younghusbandi may have diverged from other highly specialized Schizothoracine species in the Zanda basin during the Pliocene epoch, which underwent major population reduction possibly due to the drastic climate change during the last glacial period. Population analysis indicated that the ancient population might have originated upstream before gradually adapting to evolve into the populations inhabiting the mid-stream and downstream regions of the Yarlung Tsangpo River. In conclusion, the chromosome-level genome and population diversity of S. younghusbandi provide valuable genetic resources for the evolution, ecology, and conservation studies of endemic fishes on the Tibetan Plateau.

Keywords

de novo genome assembly / population genomics / Schizopygopsis younghusbandi

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Chaowei ZHOU, Yan ZHOU, Luohao XU, Fei LIU, Luo LEI, He GAO, Junting LI, Suxing FU, Yuting DUAN, Yougang TAN, Weihua MAO, Qiming WANG, Rongzhu ZHOU, Shijun XIAO, Chuan LIU, Haiping LIU. Chromosome-level genome assembly and population genomic analysis provide insights into the genetic diversity and adaption of Schizopygopsis younghusbandi on the Tibetan Plateau. Integrative Zoology, 2025, 20(6): 1246-1264 DOI:10.1111/1749-4877.12910

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References

[1]

Alexander DH, Novembre J, Lange K (2009). Fast model-based estimation of ancestry in unrelated individuals. Genome Research 19, 1655–1664.

[2]

Ben-Jemaa S, Adam G, Boussaha M et al. (2023). Whole genome sequencing reveals signals of adaptive admixture in Creole cattle. Scientific Reports 13, 12155.

[3]

Benson G (1999). Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research 27, 573–580.

[4]

Birney E, Clamp M, Durbin R (2004). GeneWise and Genomewise. Genome Research 14, 988–995.

[5]

Bonkovsky HL, Guo JT, Hou W et al. (2013). Porphyrin and heme metabolism and the porphyrias. Comprehensive Physiology 3, 365–401.

[6]

Camacho C, Coulouris G, Avagyan V et al. (2009). BLAST+: Architecture and applications. BMC Bioinformatics 10, 421.

[7]

Campàs O, Noordstra I, Yap AS (2023). Adherens junctions as molecular regulators of emergent tissue mechanics. Nature Reviews Molecular Cell Biology , 25, 252–269.

[8]

Canton J, Neculai D, Grinstein S (2013). Scavenger receptors in homeostasis and immunity. Nature Reviews Immunology 13, 621–634.

[9]

Chaisson MJ, Tesler G (2012). Mapping single molecule sequencing reads using basic local alignment with successive refinement (BLASR): Application and theory. BMC Bioinformatics 13, 238.

[10]

Chen F, Chen Y, He D (2008). Age and growth of Schizopygopsis younghusbandi younghusbandi in the Yarlung Zangbo River in Tibet, China. Environmental Biology of Fishes 86, 155–162.

[11]

Chen S, Zhou Y, Chen Y, Gu J (2018). fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34, i884–i890.

[12]

Chin CS, Alexander DH, Marks P et al. (2013). Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data. Nature Methods 10, 563–569.

[13]

Coudert E, Gehant S, De Castro E et al. (2023). Annotation of biologically relevant ligands in UniProtKB using ChEBI. Bioinformatics 39, btac793.

[14]

Danecek P, Auton A, Abecasis G et al. (2011). The variant call format and VCFtools. Bioinformatics 27, 2156–2158.

[15]

Denker SP, Barber DL (2002). Ion transport proteins anchor and regulate the cytoskeleton. Current Opinion in Cell Biology 14, 214–220.

[16]

Duan Y, Huo B, Ma B, Yang X, Xie C (2018). Reproductive biology of Schizopygopsis younghusbandi Regan 1905 (Cyprinidae: Schizothoracinae) in the middle reaches of Yarlung Tsangpo River, China. Journal of Oceanology and Limnology 36, 1825–1834.

[17]

Dudchenko O, Batra SS, Omer AD et al. (2017). De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92–95.

[18]

Durand NC, Shamim MS, Machol I et al. (2016). Juicer provides a one-click system for analyzing loop-resolution Hi-C experiments. Cell Systems 3, 95–98.

[19]

Edgar RC, Myers EW (2005). PILER: Identification and classification of genomic repeats. Bioinformatics 21, i152–i158.

[20]

Favre A, Packert M, Pauls SU et al. (2015). The role of the uplift of the Qinghai-Tibetan Plateau for the evolution of Tibetan biotas. Biological Reviews of the Cambridge Philosophical Society 90, 236–253.

[21]

Feng Z, Saha L, Dritsa C, Wan Q, Glebov OO (2022). Temperature-dependent structural plasticity of hippocampal synapses. Frontiers in Cellular Neuroscience 16, 1009970.

[22]

Fu Z, Gilbert ER, Liu D (2013). Regulation of insulin synthesis and secretion and pancreatic Beta-cell dysfunction in diabetes. Current Diabetes Reviews 9, 25–53.

[23]

Gao K, He Z, Xiong J et al. (2024). Population structure and adaptability analysis of Schizothorax o'connori based on whole-genome resequencing. BMC Genomics 25, 145.

[24]

Gong Z, Zhai D, Chen J, Liu B, Zhu T (2023). Landscape determinants of genetic structure for Schizopygopsis younghusbandi in the Yarlung Tsangpo River drainage, Tibetan Plateau. Ecological Indicators 151, 110309.

[25]

Grabherr MG, Haas BJ, Yassour M et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29, 644–652.

[26]

Grubelnik V, Zmazek J, Markovic R, Gosak M, Marhl M (2020). Modelling of energy-driven switch for glucagon and insulin secretion. Journal of Theoretical Biology 493, 110213.

[27]

Guo S-S, Zhang G-R, Guo X-Z et al. (2014). Genetic diversity and population structure of Schizopygopsis younghusbandi Regan in the Yarlung Tsangpo River inferred from mitochondrial DNA sequence analysis. Biochemical Systematics and Ecology 57, 141–151.

[28]

Haas BJ, Papanicolaou A, Yassour M et al. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nature Protocols 8, 1494–1512.

[29]

Haas BJ, Salzberg SL, Zhu W et al. (2008). Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biology 9, R7.

[30]

He DK, Chen YF (2006). Biogeography and molecular phylogeny of the genus Schizothorax (Teleostei: Cyprinidae) in China inferred from cytochrome b sequences. Journal of Biogeography 33, 1448–1460.

[31]

Jones P, Binns D, Chang HY et al. (2014). InterProScan 5: Genome-scale protein function classification. Bioinformatics 30, 1236–1240.

[32]

Kanehisa M, Goto S (2000). KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28, 27–30.

[33]

Kardos M, Luikart G, Bunch R et al. (2015). Whole-genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep. Molecular Ecology 24, 5616–5632.

[34]

Kelletat DH (2005). Pleistocene epoch. Encyclopedia of Earth Sciences Series 14, 772–773.

[35]

Kent WJ (2002). BLAT–The BLAST-like alignment tool. Genome Research 12, 656–664.

[36]

Kim D, Pertea G, Trapnell C et al. (2013). TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14, R36.

[37]

Kohany O, Gentles AJ, Hankus L, Jurka J (2006). Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics 7, 474.

[38]

Korf I (2004). Gene finding in novel genomes. BMC Bioinformatics 5, 59.

[39]

Kumar S, Suleski M, Craig JM et al. (2022). TimeTree 5: An expanded resource for species divergence times. Molecular Biology and Evolution 39, msac174.

[40]

Larkin DM, Daetwyler HD, Hernandez AG et al. (2012). Whole-genome resequencing of two elite sires for the detection of haplotypes under selection in dairy cattle. PNAS 109, 7693–7698.

[41]

Lee TH, Guo H, Wang X, Kim C, Paterson AH (2014). SNPhylo: A pipeline to construct a phylogenetic tree from huge SNP data. BMC Genomics 15, 162.

[42]

Li F, Xu Z, Feng Y, Liu M, Liu W (2013). Changes of land cover in the Yarlung Tsangpo River basin from 1985 to 2005. Environmental Earth Sciences 68, 181–188.

[43]

Li H (2013). Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv, 1303.3997.

[44]

Li H, Handsaker B, Wysoker A et al. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079.

[45]

Li Y, Burridge CP, Lv Y, Peng Z (2021). Morphometric and population genomic evidence for species divergence in the Chimarrichthys fish complex of the Tibetan Plateau. Molecular Phylogenetics and Evolution 159, 107117.

[46]

Liang Y, He D, Jia Y, Sun H, Chen Y (2017). Phylogeographic studies of schizothoracine fishes on the central Qinghai-Tibet Plateau reveal the highest known glacial microrefugia. Scientific Reports 7, 10983.

[47]

Liu HP, Xiao SJ, Wu N et al. (2019). The sequence and de novo assembly of Oxygymnocypris stewartii genome. Scientific Data 6, 190009.

[48]

Liu HP, Ye SW, Li ZJ (2016). Length–weight relationships of three schizothoracinae fish species from the Niyang River, a branch of the Yarlung Zangbo River, Tibet, China. Journal of Applied Ichthyology 32, 982–985.

[49]

Liu X, Liu W, Lenstra JA et al. (2023). Evolutionary origin of genomic structural variations in domestic yaks. Nature Communications 14, 5617.

[50]

Ma BS, Wei KJ, Zhao TY, Pei FC, Huo B (2023a). Research progress on the systematic evolution and plateau adaptation of schizothoracine fishes. Journal of Lake Sciences 35, 808–824. (In Chinese.)

[51]

Ma Q, Luo Y, Zhong J et al. (2023b). Hypoxia tolerance in fish depends on catabolic preference between lipids and carbohydrates. Zoological Research 44, 954–966.

[52]

Majoros WH, Pertea M, Salzberg SL (2004). TigrScan and GlimmerHMM: Two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879.

[53]

Manni M, Berkeley MR, Seppey M, Zdobnov EM (2021). BUSCO: Assessing genomic data quality and beyond. Current Protocols 1, e323.

[54]

Mendes FK, Vanderpool D, Fulton B, Hahn MW (2021). CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics 36, 5516–5518.

[55]

Mortazavi A, Williams BA, Mccue K, Schaeffer L, Wold B (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628.

[56]

Nakamura T, Yamada KD, Tomii K, Katoh K (2018). Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34, 2490–2492.

[57]

Niu J, Zhang R, Hu J et al. (2022). Chromosomal-scale genome assembly of the near-extinction big-head schizothorcin (Aspiorhynchus laticeps). Scientific Data 9, 556.

[58]

Park JM, Hong KI, Lee H, Jang WD (2021). Bioinspired applications of porphyrin derivatives. Accounts of Chemical Research 54, 2249–2260.

[59]

Paysan-Lafosse T, Blum M, Chuguransky S et al. (2023). InterPro in 2022. Nucleic Acids Research 51, D418–D427.

[60]

Qi D, Guo S, Chao Y et al. (2015). The biogeography and phylogeny of schizothoracine fishes (Schizopygopsis) in the Qinghai-Tibetan Plateau. Zoologica Scripta 44, 523–533.

[61]

Qi D, Guo S, Tang J, Zhao X, Liu J (2007). Mitochondrial DNA phylogeny of two morphologically enigmatic fishes in the subfamily Schizothoracinae (Teleostei: Cyprinidae) in the Qinghai-Tibetan Plateau. Journal of Fish Biology 70, 60–74.

[62]

Qian Y, Meng M, Zhou C et al. (2023). The role of introgression during the radiation of endemic fishes adapted to living at extreme altitudes in the Tibetan Plateau. Molecular Biology and Evolution 40, msad129.

[63]

Qin Z, Sun X (2023). Glacial-interglacial cycles and early human evolution in China. Land 12, 1683.

[64]

Redmond AK, Casey D, Gundappa MK, Macqueen DJ, Mclysaght A (2023). Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor. Nature Communications 14, 2879.

[65]

Shao J, Ma BS, Duan YJ et al. (2019). Population resources and fishery management policies of Schizopygopsis younghusbandi in the Yarlung Zangbo River, China. Chinese Journal of Applied Ecology 30, 2437–2446.

[66]

She R, Chu JS, Wang K, Pei J, Chen N (2009). GenBlastA: Enabling BLAST to identify homologous gene sequences. Genome Research 19, 143–149.

[67]

Stamatakis A (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.

[68]

Stanke M, Tzvetkova A, Morgenstern B (2006). AUGUSTUS at EGASP: Using EST, protein and genomic alignments for improved gene prediction in the human genome. Genome Biology 7, S11.1–S11.8.

[69]

Terhorst J, Kamm JA, Song YS (2017). Robust and scalable inference of population history from hundreds of unphased whole genomes. Nature Genetics 49, 303–309.

[70]

Thompson AW, Hawkins MB, Parey E et al. (2021). The bowfin genome illuminates the developmental evolution of ray-finned fishes. Nature Genetics 53, 1373–1384.

[71]

Tian F, Liu S, Zhou B et al. (2022). Chromosome-level genome of Tibetan naked carp (Gymnocypris przewalskii) provides insights into Tibetan highland adaptation. DNA Research 29, dsac025.

[72]

Van Der Auwera GA, Carneiro MO, Hartl C et al. (2013). From FastQ data to high confidence variant calls: The Genome Analysis Toolkit best practices pipeline. CP in Bioinformatics 43, 11.10.1–11.10.33.

[73]

Vogel A, Brunner JS, Hajto A, Sharif O, Schabbauer G (2022). Lipid scavenging macrophages and inflammation. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids 1867, 159066.

[74]

Vurture GW, Sedlazeck FJ, Nattestad M et al. (2017). GenomeScope: Fast reference-free genome profiling from short reads. Bioinformatics 33, 2202–2204.

[75]

Walker BJ, Abeel T, Shea T et al. (2014). Pilon: An integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS ONE 9, e112963.

[76]

Wang F, Wang L, Liu D et al. (2022). Chromosome-level assembly of Gymnocypris eckloni genome. Scientific Data 9, 464.

[77]

Wang K, Wang J, Zhu C et al. (2021a). African lungfish genome sheds light on the vertebrate water-to-land transition. Cell 184, 1362–1376.

[78]

Wang M, Witvliet D, Wu M, Kang L, Shao Z (2021b). Temperature regulates synaptic subcellular specificity mediated by inhibitory glutamate signaling. PLoS Genetics 17, e1009295.

[79]

Wang N, Chang M-M (2010). Pliocene cyprinids (Cypriniformes, Teleostei) from Kunlun Pass Basin, northeastern Tibetan Plateau and their bearings on development of water system and uplift of the area. Science China Earth Sciences 53, 485–500.

[80]

Wang X, Gan X, Li J, Chen Y, He S (2016). Cyprininae phylogeny revealed independent origins of the Tibetan Plateau endemic polyploid cyprinids and their diversifications related to the Neogene uplift of the plateau. Science China Life Sciences 59, 1149–1165.

[81]

Wingett S, Ewels P, Furlan-Magaril M et al. (2015). HiCUP: Pipeline for mapping and processing Hi-C data. F1000Research 4, 1310.

[82]

Wu T, Hu E, Xu S et al. (2021). clusterProfiler 4.0: A universal enrichment tool for interpreting omics data. Innovation 2, 100141.

[83]

Wu Y (1992). The Fishes of the Qinghai-Xizang Plateau. Sichuan Science and Technology Press, Chengdu, China. (In Chinese.)

[84]

Wu YF, Kang B, Men Q (1999). Chromosome diversity of tibetan fishes. Zoological Research 20, 258–264. (In Chinese.)

[85]

Xiao S, Mou Z, Fan D et al. (2020). Genome of tetraploid fish Schizothorax o'connori provides insights into early re-diploidization and high-altitude adaptation. Iscience 23, 101497.

[86]

Xiao SJ, Mou ZB, Yang RB et al. (2021). Genome and population evolution and environmental adaptation of Glyptosternon maculatum on the Qinghai-Tibet Plateau. Zoological Research 42, 502–513.

[87]

Xu Z, Wang H (2007). LTR_FINDER: An efficient tool for the prediction of full-length LTR retrotransposons. Nucleic Acids Research 35, W265–W268.

[88]

Yang L, Sun N, Zeng H et al. (2023). Enlarged fins of Tibetan catfish provide new evidence of adaptation to high plateau. Science China Life Sciences 66, 1554–1568.

[89]

Yang X (2011). Feeding habits of Schizopygopsis younghusbandi younghusbandi. Freshwater Fisheries 41, 40–44.

[90]

Yang Z (2007). PAML 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24, 1586–1591.

[91]

Yu D, Ren Y, Uesaka M et al. (2024). Hagfish genome elucidates vertebrate whole-genome duplication events and their evolutionary consequences. Nature Ecology & Evolution 8, 519–535.

[92]

Yuan D, Chen X, Gu H et al. (2020). Chromosomal genome of Triplophysa bleekeri provides insights into its evolution and environmental adaptation. Gigascience 9, giaa132.

[93]

Zhang M, Yang C, Tasan I, Zhao H (2021). Expanding the potential of mammalian genome engineering via targeted DNA integration. ACS Synthetic Biology 10, 429–446.

[94]

Zheng D (1996). The system of physico-geographical regions of the Qinghai-Xizang (Tibet) Plateau. Science China Earth Sciences 39, 410–417.

[95]

Zhou C, Xiao S, Liu Y et al. (2020). Comprehensive transcriptome data for endemic Schizothoracinae fish in the Tibetan Plateau. Scientific Data 7, 28.

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