Divergent adaptation to Qinghai-Tibetan Plateau implicated from transciptome study of Gymnocypris dobula and Schizothorax nukiangensis
Introduction
The Qinghai-Tibet Plateau (QTP) is the highest and one of the biggest plateaus on earth, covering 2.5 × 106 square kilometers with an elevation of 3000–5000 m for most parts of the area. The QTP has been uplifting since approximately 45 million years ago, resulted from collision of the India plate and the Eurasia plate (Li and Fang, 1999, Favre et al., 2014). The uplifting dramatically changed the environment conditions from an originally humid and warm climate to currently a dry and cold one (Wu et al., 2008). Characterized by factors including hypoxia, cold and strong ultraviolet radiation, the QTP environment posed harsh challenges to the endemic animals (Scheinfeldt and Tishkoff, 2010). Using comparative genomics and transcriptomics analysis, recent studies have identified various genes and signaling pathways that may be responsible for highland adaptation in both terrestrial and aquatic vertebrates. For example, genetic modifications to metabolism and cardiovascular system development are frequently found in the highland adapted animals (Qiu et al., 2012, Qu et al., 2013, Gou et al., 2014).
The family Cyprinidae is the most diverse clade in freshwater fishes (Chen and Mayden, 2009). The Schizothoracine fishes (Teleostei: Cyprinidae) dominate the lakes and rivers throughout the Tibetan Plateau and its peripheral regions. More than 70 species in twelve genera in the subfamily Schizothoracinae are endemic to the Tibetan Plateau (He and Chen, 2006). According to the degree of specialization of their morphological traits, the Schizothoracine fishes are divided into three grades: Primitive, specialized, and highly specialized, with Primitive ones live in the peripheral regions at around 1000 m above sea level (a.s.l) and the other two groups are intermingled with each other in the central part of QTP at above 3000 m a.s.l (He and Chen, 2006, Qi et al., 2012).
Recent transcriptome studies on Schizothoracines and other endemic Tibetan fishes have identified multiple biological processes and genes involved in highland adaptation, including genes that participate in metabolic processes and responses to hypoxia (Yang et al., 2014, Ma et al., 2015). Despite great progresses made in these investigations, most of current studies are limited to single highland species with comparisons made to distantly related teleosts. Such comparisons are limited in power to decipher the detailed molecular adaptations associated with Schizothoracine expansion in QTP. Therefore, genome-wide investigations of adaptive signals among Schizothoracine species of differently graded specialization are highly demanded to further reveal the genetic mechanisms of adaptation in these fishes.
The objective of this study was to carry out a comparative genome-wide screen for genes that might be involved in highland adaptation from species living at different altitudes. To achieve these aims, we generated transcriptomes of a primitive Schizothoracine fish Schizothorax nukiangensis Tsao, which lives at about 1,000 m a.s.l, and a highly specialized one Gymnocypris dobula which lives at 3000–4000 m a.s.l, and we performed evolutionary analyses on these data.
Section snippets
Ethics statement
This study was approved by the Ethics Committee for the Use of Animal Subjects of Shanghai Ocean University.
Sample collection, cDNA library construction and illumina sequencing
G. dobula was collected from Lake Duoqing, situated at eastern QTP (28°03.37′, 89°17.83′) with an altitude of 4509 m a.s.l, and a temperature at 11.0 °C, the concentration of dissolved oxygen in the water was 1.9 mg/L; while S. nukiangensis was collected from Nujiang, Yunnan, situated on the eastern margin of QTP (25°41.24’, 98°53.22), with an altitude of 1201 m a.s.l and at a temperature
De novo assembly and annotation of transcriptomes
RNA-sequencing generated 188.70 million raw reads in about 94 Gb of data from S. nukiangensis, and 198.82 million raw reads in about 98 Gb of data of G. dobula. The original sequencing data were deposited in the NCBI and can be accessed in the Short Read Archive (SRA) under the accession numbers (SRP094994 and SRP095655). De novo assembly of these reads generated 91,854 unigenes for G. dobula and 171,555 unigenes for S. nukiangensis. The N50s of the two datasets are 1665 bp and 1661 bp,
Discussion
In this study, we performed multi-tissue transcriptome sequencing of two Schizothoracine fishes and found many genes and functions might be involved in highland adaptation for these fishes.
As increased evolutionary rates of genes are regarded as signals of adaptive evolution at molecular level, we investigated the evolutionary rates of Schizothoracines by estimating dN/dS ratios. We found that dN/dS ratios of both Schizothoracines were significantly higher than that of zebrafish. Our results
Acknowledgement
This work was supported in part by the National Natural Science Foundation of China (31130049), the Research Project of the Chinese Ministry of Education (no. 213013A), the National Natural Science Foundation of China (grant no. 31572598), the “Shuguang Program” supported by the Shanghai Education Development Foundation and the Shanghai Municipal Education Commission (grant no. 13SG51), and the Shanghai Municipal Project for First-Class Discipline of Fishery to Shanghai Ocean University.
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Hb adaptation to hypoxia in high-altitude fishes: Fresh evidence from schizothoracinae fishes in the Qinghai-Tibetan Plateau
2021, International Journal of Biological MacromoleculesCitation Excerpt :However, the evolutionary process of schizothoracinae fishes is clearly related to specific periods of the geological evolution of the QTP and they have eventually evolved to adapt to the water environments [14,15,18]. Moreover, schizothoracinae fishes are considered to be polyploidy because of the complex chromosome compositions, which partly contribute to the evolutionary adaptation of the high-altitude hypoxia [21–25]. The physiologically acclimatization of organisms to environmental O2 availability is ultimately reflected in the balance of O2 demand (metabolism) and supply (uptake and transport) [26–28].
Research progress on the systematic evolution and plateau adaptation of schizothoracine fishes
2023, Hupo Kexue/Journal of Lake SciencesHypoxia-inducible factor 1α from a high-altitude fish enhances cytoprotection and elevates nitric oxide production in hypoxic environment
2020, Fish Physiology and BiochemistryHistology and ultrastructure of the gill in the teleost Schizothorax nukiangensis
2018, Journal of Fishery Sciences of China
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These authors contributed equally.