Convergent molecular evolution of thermogenesis and circadian rhythm in Arctic ruminants

Author:

Li Manman1ORCID,Li Xinmei1,Wu Zhipei1,Zhang Guanghui2,Wang Nini1ORCID,Dou Mingle1ORCID,Liu Shanlin3ORCID,Yang Chentao4ORCID,Meng Guanliang5ORCID,Sun Hailu4ORCID,Hvilsom Christina6ORCID,Xie Guoxiang1,Li Yang1,Li Zhuo hui1,Wang Wei1ORCID,Jiang Yu1ORCID,Heller Rasmus7ORCID,Wang Yu12ORCID

Affiliation:

1. Key Laboratory of Animal Genetics, Breeding and Reproduction of Shaanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling 712100, People's Republic of China

2. Key Laboratory of Animal Biotechnology, Ministry of Agriculture and Rural Affairs, Northwest A&F University, Yangling 712100, People's Republic of China

3. Department of Entomology, China Agricultural University, West Yuanmingyuan Road, Beijing 100193, People's Republic of China

4. BGI Shenzhen, Shenzhen 518083, People's Republic of China

5. Centre of Taxonomy and Evolutionary Research, Zoological Research Museum Alexander Koenig, 53113 Bonn, Germany

6. Copenhagen Zoo, 2000 Frederiksberg, Denmark

7. Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, 2100 Copenhagen, Denmark

Abstract

The muskox and reindeer are the only ruminants that have evolved to survive in harsh Arctic environments. However, the genetic basis of this Arctic adaptation remains largely unclear. Here, we compared a de novo assembled muskox genome with reindeer and other ruminant genomes to identify convergent amino acid substitutions, rapidly evolving genes and positively selected genes among the two Arctic ruminants. We found these candidate genes were mainly involved in brown adipose tissue (BAT) thermogenesis and circadian rhythm. Furthermore, by integrating transcriptomic data from goat adipose tissues (white and brown), we demonstrated that muskox and reindeer may have evolved modulating mitochondrion, lipid metabolism and angiogenesis pathways to enhance BAT thermogenesis. In addition, results from co-immunoprecipitation experiments prove that convergent amino acid substitution of the angiogenesis-related gene hypoxia-inducible factor 2alpha ( HIF2A ), resulting in weakening of its interaction with prolyl hydroxylase domain-containing protein 2 (PHD2), may increase angiogenesis of BAT. Altogether, our work provides new insights into the molecular mechanisms involved in Arctic adaptation.

Funder

Postdoctoral Innovative Talents Support Program of China

National Natural Science Foundation of China

High-Performance Computing Center

Northwest A&F University

Research and Development Program of China

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Environmental Science,General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine

Cited by 2 articles. 订阅此论文施引文献 订阅此论文施引文献,注册后可以免费订阅5篇论文的施引文献,订阅后可以查看论文全部施引文献

1. Convergent genomics and Arctic adaptation of ruminants;Proceedings of the Royal Society B: Biological Sciences;2024-01-03

2. Population genomics of the muskox' resilience in the near absence of genetic variation;Molecular Ecology;2023-11-16

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