Genome and population evolution and environmental adaptation of Glyptosternon maculatum on the Qinghai-Tibet Plateau

Zool Res. 2021 Jul 18;42(4):502-513. doi: 10.24272/j.issn.2095-8137.2021.096.

Abstract

Persistent uplift means the Qinghai-Tibet Plateau (QTP) is an ideal natural laboratory to investigate genome evolution and adaptation within highland environments. However, how paleogeographic and paleoclimatic events influence the genome and population of endemic fish species remains unclear. Glyptosternon maculatum is an ancient endemic fish found on the QTP and the only critically endangered species in the Sisoridae family. Here, we found that major transposons in the G. maculatum genome showed episodic bursts, consistent with contemporaneous geological and climatic events during the QTP formation. Notably, histone genes showed significant expansion in the G. maculatum genome, which may be mediated by long interspersed nuclear elements (LINE) repetitive element duplications. Population analysis showed that ancestral G. maculatum populations experienced two significant depressions 2.6 million years ago (Mya) and 10 000 years ago, exhibiting excellent synchronization with Quaternary glaciation and the Younger Dryas, respectively. Thus, we propose that paleogeography and paleoclimate were dominating driving forces for population dynamics in endemic fish on the QTP. Tectonic movements and temperature fluctuation likely destroyed the habitat and disrupted the drainage connectivity among populations. These factors may have caused severe bottlenecks and limited migration among ancestral G. maculatum populations, resulting in the low genetic diversity and endangered status of the species today.

持续的海拔抬升使得青藏高原成为了研究基因组进化和高原环境适应性理想的“天然实验室”。目前,尚不清楚古地理和古气候是如何影响高原特色鱼类的基因组和群体进化的。黑斑原鮡是一种青藏高原特有的极危鮡科鱼类。该研究发现黑斑原鮡基因组内的主要转座子序列发生了周期性地扩张,扩张的时间与青藏高原形成过程中的主要地理和气候时间高度吻合。更有意思的是,黑斑原鮡基因组内的组蛋白发生了大量扩张,研究发现组蛋白的扩张可能是由于LINE重复序列复制介导的。群体研究表明,黑斑原鮡群体分别在约260万年和1万年前经历了二次大规模的种群衰退,时间上与第四季末次冰期和新仙女木事件时间一致。因此,我们推测青藏高原的古地理和古气候是高原鱼类基因组和群体进化的主要推动力。古地质运动和气候波动都可以破坏和改变原始高原鱼类赖以生存的栖息地和水系,从而导致了黑斑原鮡群体的瓶颈效应并限制了群体之间的基因交流,这有可能就是目前黑斑原鮡群体遗传多样性较低和处于极危状态的原因。.

Keywords: Genome evolution; Glyptosternon maculatum; High-altitude adaptation; Population; Qinghai-Tibet Plateau (QTP).

MeSH terms

  • Adaptation, Physiological*
  • Animals
  • Biological Evolution*
  • Climate
  • Ecosystem*
  • Fishes / genetics*
  • Genome*
  • Tibet

Associated data

  • BioProject/PRJNA447978
  • SRA/SRR7268130–SRR7268162

Grants and funding

This project was supported by the Key Research and Development Projects in Tibet: Preservation of Characteristic Biological Germplasm Resources and Utilization of Gene Technology in Tibet (XZ202001ZY0016N), National Natural Science Foundation of China (32072980), and Special Finance of Tibet Autonomous Region (XZNKY-2019-C-053)