Adaptive Transcriptome Profiling of Subterranean Zokor, Myospalax baileyi, to High- Altitude Stresses in Tibet

Zhenyuan Cai,Liuyang Wang,Somnath Tagore,Xiaoying Song,Zeev Frenkel,Tongzuo Zhang,Milana Frenkel-Morgenstern,Jiarui Chen,Kexin Li,Xiangfeng Li,Eviatar Nevo,Dahai Gao,Huihua Wang

doi:10.1038/s41598-018-22483-7

Abstract

Animals living at high altitudes have evolved distinct phenotypic and genotypic adaptations against stressful environments. We studied the adaptive patterns of altitudinal stresses on transcriptome turnover in subterranean plateau zokors (Myospalax baileyi) in the high-altitude Qinghai-Tibetan Plateau. Transcriptomes of zokors from three populations with distinct altitudes and ecologies (Low: 2846 m, Middle: 3282 m, High: 3,714 m) were sequenced and compared. Phylogenetic and principal component analyses classified them into three divergent altitudinal population clusters. Genetic polymorphisms showed that the population at H, approaching the uppermost species boundary, harbors the highest genetic polymorphism. Moreover, 1056 highly up-regulated UniGenes were identified from M to H. Gene ontologies reveal genes like EPAS1 and COX1 were overexpressed under hypoxia conditions. EPAS1, EGLN1, and COX1 were convergent in high-altitude adaptation against stresses in other species. The fixation indices (FST and GST)-based outlier analysis identified 191 and 211 genes, highly differentiated among L, M, and H. We observed adaptive transcriptome changes in Myospalax baileyi, across a few hundred meters, near the uppermost species boundary, regardless of their relatively stable underground burrows’ microclimate. The highly variant genes identified in Myospalax were involved in hypoxia tolerance, hypercapnia tolerance, ATP-pathway energetics, and temperature changes.

Highlights

Zokors, genus Myospalax, are burrowing rodents that resemble mole rats, Spalax
The brain was chosen as the study organ as it is known to be highly sensitive to hypoxia
As stresses like cold temperature, low-food resources, high UV, high hypoxia, and hypercapnia are extreme at the high altitudes, many genes are expected to be involved in the adaptation, especially near the highest species border (4,600 m)

Summary

Introduction

Like the Myospalax baileyi in Tibet, environmental stresses play a major role in their adaptive evolution[1] Though they reside underground, Tibetan plateau zokors may have transcriptomic changes that might correlate with altitude. High-altitude stresses like solar radiation, hypoxia, hypercapnia, low temperature, and food shortage work in concert imposing interactive physiological challenges on these organisms. We identified 1,056 differentially expressed genes whose expression was upregulated upward across the short distance of 432 m from M to H We hypothesize that this increase in upregulation upward resists some of the high Tibetan altitudinal stresses (solar radiation, cold temperature, hypoxia, and food scarcity). We showed that natural selection, which was substantiated statistically, has adaptively molded zokor’s transcriptome between distinctly divergent populations of the same subterranean rodent species, Myospalax baileyi, and across a few hundred meters, to adaptively and effectively cope with Qinghai-Tibetan Plateau altitudinal stresses

Methods

Results

Discussion

Conclusion