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

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.

SUBMITTER: Xiao SJ

PROVIDER: S-EPMC8317186 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMolecular adaptation to the severe environments present during the uplift of the Qinghai-Tibet Plateau has attracted the attention of researchers. The divergence of the three specialization groups of schizothoracins (Primitive, Specialized and Highly Specialized) may correspond to the three phases of plateau uplift. Based on the transcripts of representative species of the three specialized groups and an outgroup, genes in schizothoracins that may have played important roles during the adaptation to new environments were investigated.ResultsThe contigs of Gymnodiptychus dybowskii and Schizothorax pseudaksaiensis were compared with those of Gymnocypris przewalskii ganzihonensis and the outgroup Sinocyclocheilus angustiporus, and 5,894 ortholog groups with an alignment length longer than 90 nt after deleting gaps were retained. Evolutionary analyses indicated that the average evolutionary rate of the branch leading to the Specialized group was faster than that of the branch leading to the Highly Specialized group. Moreover, the numbers of gene categories in which more than half of the genes evolved faster than the average values of the genome were 117 and 15 along the branches leading to the Specialized and Highly Specialized groups, respectively. A total of 40, 36, and 55 genes were likely subject to positive selection along the branches leading to the Primitive, Specialized and Highly Specialized groups, respectively, and many of these genes are likely relevant to adaptation to the cold temperatures, low oxygen concentrations, and strong ultraviolet radiation that result from elevation.ConclusionsBy selecting representative species of the three groups of schizothoracins and applying next-generation sequencing technology, several candidate genes corresponding to adaptation to the three phases of plateau uplift were identified. Some of the genes identified in this report that were likely subject to positive selection are good candidates for subsequent evolutionary and functional analyses of adaptation to high altitude.

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

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