Molecular Mechanisms of Spawning Habits for the Adaptive Radiation of Endemic East Asian Cyprinid Fishes
Feng Chen,
Yeke Wang,
Jun He,
Liang Chen,
Ge Xue,
Yan Zhao,
Yanghui Peng,
Carl Smith,
Jia Zhang,
Jun Chen,
Ping Xie
Affiliations
Feng Chen
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Yeke Wang
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Jun He
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
Liang Chen
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
Ge Xue
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Yan Zhao
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Yanghui Peng
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Carl Smith
Department of Ecology and Vertebrate Zoology, University of Łódź, Łódź, Poland; Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic
Jia Zhang
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; University of Chinese Academy of Sciences, Beijing 100049, China
Jun Chen
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China
Ping Xie
Donghu Experimental Station of Lake Ecosystems, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China; Institute of Ecological Research and Pollution Control of Plateau Lakes, School of Ecology and Environment, Yunnan University, Kunming 650500, China
Despite the widespread recognition of adaptive radiation as a driver of speciation, the mechanisms by which natural selection generates new species are incompletely understood. The evolutionary radiation of endemic East Asian cyprinids has been proposed as evolving through a change in spawning habits, involving a transition from semibuoyant eggs to adhesive eggs in response to crosslinked river-lake system formation. Here, we investigated the molecular mechanisms that underpin this radiation, associated with egg hydration and adhesiveness. We demonstrated that semibuoyant eggs enhance hydration by increasing the degradation of yolk protein and accumulation of Ca2+ and Mg2+ ions, while adhesive eggs improve adhesiveness and hardness of the egg envelope by producing an adhesive layer and a unique 4th layer to the egg envelope. Based on multiomics analyses and verification tests, we showed that during the process of adaptive radiation, adhesive eggs downregulated the “vitellogenin degradation pathway,” “zinc metalloprotease pathway,” and “ubiquitin-proteasome pathway” and the pathways of Ca2+ and Mg2+ active transport to reduce their hydration. At the same time, adhesive eggs upregulated the crosslinks of microfilament-associated proteins and adhesive-related proteins, the hardening-related proteins of the egg envelope, and the biosynthesis of glycosaminoglycan in the ovary to generate adhesiveness. These findings illustrate the novel molecular mechanisms associated with hydration and adhesiveness of freshwater fish eggs and identify critical molecular mechanisms involved in the adaptive radiation of endemic East Asian cyprinids. We propose that these key egg attributes may function as “magic traits” in this adaptive radiation.