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.
Highlights
Animals living in different habitats are affected by various ecological factors such as photoperiod, food quantity or quality, and temperature (Van Beest et al, 2012; Hanya and Chapman, 2013; Olanrewaju et al, 2013)
No significant difference was observed in gene expression between the sexes (F 0.36, p > 0.05), whereas significant differences were detected between the three altitudes (F 15.56, p < 0.05)
The expression levels of pgc-1α, pparα, and PR domain-containing 16 (PRDM16) genes in the white adipose tissue (WAT) and brown adipose tissue (BAT) of plateau pikas from high- and mediumaltitude regions were significantly higher than those from the low-altitude region (p < 0.05; Figures 2A,C)
Summary
Animals living in different habitats are affected by various ecological factors such as photoperiod, food quantity or quality, and temperature (Van Beest et al, 2012; Hanya and Chapman, 2013; Olanrewaju et al, 2013). As ambient temperature decreases, animals may adjust their behavior and/or physiology to reduce their energy expenditure (Humphries et al, 2005; Zub et al, 2009). Animals such as Mustela nivalis, Spermophilus parryii, and Rhabdomys pumilio can huddle together or stay in the nest to conserve energy and maintain body temperature (Geiser, 2004; Scantlebury et al, 2006; Sukhchuluun et al, 2018). Studies on Anolis carolinensis, Rhinopithecus bieti, Thermophis baileyi, and Sus scrofa have uncovered the gene-expression mechanisms underlying their behavioral and physiological adaptations (Li et al, 2013; Yu et al, 2016; Li T. et al, 2018; Kabelik et al, 2021)
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