Differential Expression of Metabolism-Related Genes in Plateau Pika (Ochotona curzoniae) at Different Altitudes on the Qinghai–Tibet Plateau

Abstract

According to life history theory, animals living in extreme environments have evolved specific behavioral and physiological strategies for survival. However, the genetic mechanisms underpinning these strategies are unclear. As the highest geographical unit on Earth, the Qinghai–Tibet Plateau is characterized by an extreme environment and climate. During long-term evolutionary processes, animals that inhabit the plateau have evolved specialized morphological and physiological traits. The plateau pika (Ochotona curzoniae), one of the native small mammals that evolved on the Qinghai–Tibet Plateau, has adapted well to this cold and hypoxic environment. To explore the genetic mechanisms underlying the physiological adaptations of plateau pika to extremely cold ambient temperatures, we measured the differences in resting metabolic rate (RMR) and metabolism-related gene expression in individuals inhabiting three distinct altitudes (i.e., 3,321, 3,663, and 4,194 m). Results showed that the body mass and RMR of plateau pika at high- and medium-altitudes were significantly higher than those at the low-altitude. The expression levels of peroxisome proliferator-activated receptor α (pparα), peroxisome proliferator-activated receptor-γ coactivator-1α (pgc-1α), and the PR domain-containing 16 (PRDM16) in white (WAT) and brown (BAT) adipose tissues of plateau pika from high- and medium-altitudes were significantly higher than in pika from the low-altitude region. The enhanced expression levels of pgc-1α and pparα genes in the WAT of pika at high-altitude showed that WAT underwent “browning” and increased thermogenic properties. An increase in the expression of uncoupling protein 1 (UCP1) in the BAT of pika at high altitude indicated that BAT increased their thermogenic properties. The gene expression levels of pparα and pgc-1α in skeletal muscles were significantly higher in high-altitude pika. Simultaneously, the expression of the sarcolipin (SLN) gene in skeletal muscles significantly increased in high-altitude pika. Our results suggest that plateau pika adapted to an extremely cold environment via browning WAT, thereby activating BAT and enhancing SLN expression to increase non-shivering thermogenesis. This study demonstrates that plateau pika can increase thermogenic gene expression and energy metabolism to adapt to the extreme environments on the plateau.

Transcriptome analysis of pika heart tissue reveals mechanisms underlying the adaptation of a keystone species on the roof of the world

“…In this study, considering that gender differences will affect the results, we used the results of heart tissue expression of Gansu pika (including five females and nine males) to analyse the differences between different genders, and the results showed that there was no significant difference. Other transcription studies of pika heart and lung tissue have also not considered the effect of gender on the results ( Zhang et al, 2022 ; Zhu et al, 2022 ). Therefore, instead of sex typing of plateau pikas and Gansu pikas, we directly analysed the transcriptome of heart tissues of 28 samples in order to explore the potential genetic mechanism of plateau pikas adapting to high altitude environment.…”

“…Qi et al (2008) showed that plateau pikas can improve their adaptation to anoxic environments by increasing the density of heart mitochondria and the microvasculature and myoglobin contents. Zhu et al (2021) measured the resting metabolic rate and transcriptional expression levels of adipose tissue, liver and skeletal muscle in pikas along different elevation gradients and proved that plateau pikas could adapt to the extreme environment of the QHTP through increases in the expression of thermogenesis genes and energy metabolism. However, current research on the high-altitude adaptation of pikas is mainly focused on nonshivering thermogenesis ( Wang et al, 1999 ; Wang et al, 2006 ), the regulation of skeletal muscle lactate dehydrogenase-c, liver hypoxia and pulmonary circulation ( Liu et al, 2012 ; Melo Ferreira et al, 2015 ; Pichon et al, 2015 ; Zhu et al, 2021 ).…”

“… Zhu et al (2021) measured the resting metabolic rate and transcriptional expression levels of adipose tissue, liver and skeletal muscle in pikas along different elevation gradients and proved that plateau pikas could adapt to the extreme environment of the QHTP through increases in the expression of thermogenesis genes and energy metabolism. However, current research on the high-altitude adaptation of pikas is mainly focused on nonshivering thermogenesis ( Wang et al, 1999 ; Wang et al, 2006 ), the regulation of skeletal muscle lactate dehydrogenase-c, liver hypoxia and pulmonary circulation ( Liu et al, 2012 ; Melo Ferreira et al, 2015 ; Pichon et al, 2015 ; Zhu et al, 2021 ). The role and adaptive mechanisms of cardiac tissue in extreme environments are less well studied, and most of the relevant previous studies have been focused on single species of pikas, without intraspecific and interspecific comparisons.…”

Effect of chronic traffic noise on behavior and physiology of plateau pikas (Ochotona curzoniae)

“…Four rounds of metabolism were measured in 120 min, with each round lasting for 30 min. We obtained the average of the lowest consecutive records as the RMR (Zhu et al, 2021).…”

Diet and high altitude strongly drive convergent adaptation of gut microbiota in wild macaques, humans, and dogs to high altitude environments

“…Meanwhile, in vertebrates, gut microbiota compositional differences among species are positively correlated with the evolutionary divergence time of the host, and the gut microbiota composition is more similar within host species than among species (Moeller et al, 2017;Song et al, 2020;Dillard et al, 2022). Additionally, environmental factors have been confirmed to be closely related to the gut microbiota structure (Ley et al, 2008;Zhao et al, 2018) and the extreme cold, the dry, hostile climate of high altitude environments, high ultraviolet radiation, and low oxygen content have important effects on the cardiovascular system, energy metabolism, and body temperature retention of animals (Simonson et al, 2010;Yu et al, 2016;Zhu et al, 2021). A variety of mammalian gut microbiota also respond to this environmental pressure, forming a composition of gut microbiota that adapts to the high altitude environments, and play an important role in host food digestion, energy metabolism, nutritional homeostasis, immune regulation, signal transduction, and other physiological activities (Bäckhed et al, 2005;Ley et al, 2006;Yan et al, 2021).…”