Temperature acclimation in hot-spring snakes and the convergence of cold response

Chaochao Yan; Wei Wu; Wenqi Dong; Bicheng Zhu; Jiang Chang; Yunyun Lv; Shilong Yang; Jia-Tang Li

doi:10.1016/j.xinn.2022.100295

Temperature acclimation in hot-spring snakes and the convergence of cold response

Innovation (Camb). 2022 Aug 1;3(5):100295. doi: 10.1016/j.xinn.2022.100295. eCollection 2022 Sep 13.

Authors

Chaochao Yan¹, Wei Wu^{1

2}, Wenqi Dong³, Bicheng Zhu¹, Jiang Chang⁴, Yunyun Lv^{1

5}, Shilong Yang³, Jia-Tang Li^{1

2

6}

Affiliations

¹ CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization and Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China.
² University of Chinese Academy of Sciences, Beijing 100049, China.
³ College of Wildlife and Protected Area, Northeast Forestry University, Harbin 660223, China.
⁴ State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100085, China.
⁵ College of Life Science, Neijiang Normal University, Neijiang, Sichuan 641100, China.
⁶ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming 650223, China.

Abstract

Animals have evolved sophisticated temperature-sensing systems and mechanisms to detect and respond to ambient temperature changes. As a relict species endemic to the Qinghai-Tibet Plateau, hot-spring snake (Thermophis baileyi) survived the dramatic changes in climate that occurred during plateau uplift and ice ages, providing an excellent opportunity to explore the evolution of temperature sensation in ectotherms. Based on distributional information and behavioral experiments, we found that T. baileyi prefer hot-spring habitats and respond more quickly to warmth than other two snakes, suggesting that T. baileyi may evolve an efficient thermal-sensing system. Using high-quality chromosome-level assembly and comparative genomic analysis, we identified cold acclimation genes experiencing convergent acceleration in high-altitude lineages. We also discovered significant evolutionary changes in thermosensation- and thermoregulation-related genes, including the transient receptor potential (TRP) channels. Among these genes, TRPA1 exhibited three species-specific amino acid replacements, which differed from those found in infrared imaging snakes, implying different temperature-sensing molecular strategies. Based on laser-heating experiments, the T. baileyi-specific mutations in TRPA1 resulted in an increase in heat-induced opening probability and thermal sensitivity of the ion channels under the same degree of temperature stimulation, which may help the organism respond to temperature changes more quickly. These results provide insight into the genetic mechanisms underpinning the evolution of temperature-sensing strategies in ectotherms as well as genetic evidence of temperature acclimation in this group.

Keywords: TRP channel; comparative genomics; hot-spring snake; thermoregulation; thermosensation.