Spatially resolved single-cell atlas reveals the macroevolutionary trajectory of animal hearts
Abstract
Animal hearts display diverse anatomical structures during adaptive evolution. Here, we present a multi-omics atlas of adult hearts from 27 species across chordates, arthropods, and mollusks. Joint analysis indicates that Bilateria hearts share a core gene repertoire, taking a stepwise “add-on” approach as a universal evolutionary strategy. The proto-heart is populated by key cell types, including cardiomyocytes, fibroblasts, endothelial, and neural cells, which maintained core signatures while evolving with shifts in living environments and corresponding adaptations in the cardiovascular system. Additionally, we reveal an evolutionarily conserved cardiomyocyte state dynamic potentially linked to cardiac development and stress responses. Finally, we identify a common molecular program underpinning chamber evolution from a ventricular foundation. Together, this work establishes a resource for understanding the intrinsic mechanisms of heart evolution.
Article Details
Journal Info
Science
American Association for the Advancement of Science
Authors (64)
Shanshan Lian
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Wei Wang
Yaoxin Liu
Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China.
Meina Lu
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Wentao Han
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Jiaxin Luo
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Xuejiao Zhang
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Yue Pang
College of Life Science, Liaoning Normal University, Dalian, China.
Yuru Li
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Yufeng Li
Xin Dang
State Key Laboratory of Natural and Biomimetic Drugs, Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, Institute of Advanced Clinical Medicine, Center for Life Sciences, College of Future Technology, Peking University, Beijing, China.
Peiyan Wang
School of Basic Medicine, Qingdao University, Qingdao, China.
Yating Qin
BGI Research, Qingdao, China.
Ning Tan
Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China.
Fang Zhang
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Jin Zhang
Shuai Gao
Women and Children’s Hospital of Qingdao University, Qingdao, China.
Runyi Zhang
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Lidong Guo
BGI Research, Qingdao, China.
Lei Jiang
Pengchong Zhang
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Yuehuan Zhang
South China Sea Institute of Oceanology, Chinese Academy of Science, Guangzhou, China.
Zhe Qu
Shanshan Pan
BGI Research, Qingdao, China.
Yue Zhang
Naina Hu
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Yadong Chen
BGI Research, Qingdao, China.
Yun Cao
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Wenbin Li
College of Life Science, Liaoning Normal University, Dalian, China.
Xiaomei Chen
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Junjie Shi
BGI Research, Qingdao, China.
Shuaiqi Yang
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Yiran Li
Qiuyun Song
BGI Research, Qingdao, China.
Lisui Bao
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Yuli Li
Xiawei Liu
BGI Research, Qingdao, China.
Jing Wang
Hunan Cancer Hospital Changsha China
Lingling Zhang
Rui Li
Xin Yu
BGI Research, Qingdao, China.
Tao Yang
Jing Chen
Ling Li
Mengqi Zhang
Lei Li
Ruihua Zhang
BGI Research, Qingdao, China.
Hongyan Li
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Ying Gu
BGI Research, Shenzhen, China.
Xun Xu
Huanming Yang
BGI Research, Shenzhen, China.
Zhenmin Bao
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
C. Geoffrey Burns
Division of Basic and Translational Cardiovascular Research, Department of Cardiology, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA.
Caroline E. Burns
Division of Basic and Translational Cardiovascular Research, Department of Cardiology, Boston Children’s Hospital, Harvard Medical School, Boston, MA, USA.
Robert G. Kelly
Aix-Marseille Université, CNRS UMR 7288, IBDM, Turing Centre for Living Systems, Marseille, France.
Jianxun Wang
School of Basic Medicine, Qingdao University, Qingdao, China.
Yang Zhao
Ying Su
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.
Guangyi Fan
BGI Research, Qingdao, China.
Qun Liu
BGI Research, Qingdao, China.
Shi Wang
Fang Zongxi Center for Marine Evo-Devo and MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao, China.
Ji-Feng Fei
Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital, Guangdong Academy of Medical Sciences, Guangzhou, China.
Silin Pan
Women and Children’s Hospital of Qingdao University, Qingdao, China.
Long Zhao
Key Laboratory of Evolution and Marine Biodiversity (Ministry of Education) and Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China.