Genomic basis of evolutionary adaptation in a warm-blooded fish

Xin Wang; Meng Qu; Yali Liu; Ralf F Schneider; Yue Song; Zelin Chen; Hao Zhang; Yanhong Zhang; Haiyan Yu; Suyu Zhang; Dongxu Li; Geng Qin; Shaobo Ma; Jia Zhong; Jianping Yin; Shuaishuai Liu; Guangyi Fan; Axel Meyer; Dazhi Wang; Qiang Lin

doi:10.1016/j.xinn.2021.100185

Genomic basis of evolutionary adaptation in a warm-blooded fish

Innovation (Camb). 2021 Nov 11;3(1):100185. doi: 10.1016/j.xinn.2021.100185. eCollection 2022 Jan 25.

Authors

Xin Wang^{1

2}, Meng Qu^{1

2}, Yali Liu^{1

2}, Ralf F Schneider³, Yue Song⁴, Zelin Chen^{1

2}, Hao Zhang^{1

2

5}, Yanhong Zhang^{1

2}, Haiyan Yu¹, Suyu Zhang⁴, Dongxu Li⁵, Geng Qin^{1

2}, Shaobo Ma^{1

2}, Jia Zhong^{1

2}, Jianping Yin^{1

2}, Shuaishuai Liu^{1

2}, Guangyi Fan^{4

6}, Axel Meyer⁷, Dazhi Wang⁵, Qiang Lin^{1

2

8

9}

Affiliations

¹ CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China.
² Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 511458, China.
³ Marine Evolutionary Ecology, GEOMAR Helmholtz Centre for Ocean Research Kiel, 24105 Kiel, Germany.
⁴ BGI-Qingdao, Qingdao 266555, China.
⁵ State Key Laboratory of Marine Environmental Science/College of the Environment and Ecology, Xiamen University, Xiamen 361102, China.
⁶ BGI-Shenzhen, Shenzhen 518083, China.
⁷ Department of Biology, University of Konstanz, Konstanz 78464, Germany.
⁸ University of the Chinese Academy of Sciences, Beijing 100101, China.
⁹ Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China.

Abstract

Few fishes have evolved elevated body temperatures compared with ambient temperatures, and only in opah (Lampris spp) is the entire body affected. To understand the molecular basis of endothermy, we analyzed the opah genome and identified 23 genes with convergent amino acid substitutions across fish, birds, and mammals, including slc8b1, which encodes the mitochondrial Na⁺/Ca²⁺ exchanger and is essential for heart function and metabolic heat production. Among endothermic fishes, 44 convergent genes with suggestive metabolic functions were identified, such as glrx3, encoding a crucial protein for hemoglobin maturation. Numerous genes involved in the production and retention of metabolic heat were also found to be under positive selection. Analyses of opah's unique inner-heat-producing pectoral muscle layer (PMI), an evolutionary key innovation, revealed that many proteins were co-opted from dorsal swimming muscles for thermogenesis and oxidative phosphorylation. Thus, the opah genome provides valuable resources and opportunities to uncover the genetic basis of thermal adaptations in fish.

Keywords: convergent evolution; endothermy; opah; thermogenesis; whole-genome sequencing.