Yulong Liu1,2,9, Gang Zhai1,9, Jingzhi Su3,9, Yulong Gong1, Bingyuan Yang4, Qisheng Lu1,2, Longwei Xi1, Yutong Zheng1,2, Jingyue Cao1,2, Haokun Liu1, Junyan Jin1, Zhimin Zhang1, Yunxia Yang1, Xiaoming Zhu1, Zhongwei Wang1,5, Gaorui Gong6, Jie Mei5,6, Zhan Yin1, Rodolphe E. Gozlan7, Shouqi Xie1,2,8 and Dong Han1,2,5 1State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei 430072, China; 2College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing 100049, China; 3Wuhan DaBeiNong (DBN) Aquaculture Technology Company Limited, Wuhan, Hubei 430090, China; 4Department of Infectious Diseases and Public Health, Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Kowloon, Hong Kong 999077, China; 5Hubei Hongshan Laboratory, Wuhan, Hubei 430070, China; 6College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei 430070, China; 7ISEM, Université de Montpellier, CNRS, IRD, 34090 Montpellier, France; 8The Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing 100049, China

↵9 These authors contributed equally to this work.

Corresponding authors: sqxieihb.ac.cn, hand21cnihb.ac.cn Abstract

Fish show variation in feeding habits to adapt to complex environments. However, the genetic basis of feeding preference and the corresponding metabolic strategies that differentiate feeding habits remain elusive. Here, by comparing the whole genome of a typical carnivorous fish (Leiocassis longirostris Günther) with that of herbivorous fish, we identify 250 genes through both positive selection and rapid evolution, including taste receptor taste receptor type 1 member 3 (tas1r3) and trypsin. We demonstrate that tas1r3 is required for carnivore preference in tas1r3-deficient zebrafish and in a diet-shifted grass carp model. We confirm that trypsin correlates with the metabolic strategies of fish with distinct feeding habits. Furthermore, marked alterations in trypsin activity and metabolic profiles are accompanied by a transition of feeding preference in tas1r3-deficient zebrafish and diet-shifted grass carp. Our results reveal a conserved adaptation between feeding preference and corresponding metabolic strategies in fish, and provide novel insights into the adaptation of feeding habits over the evolution course.

Footnotes

[Supplemental material is available for this article.]

Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.278476.123.

Freely available online through the Genome Research Open Access option.

Received September 6, 2023. Accepted July 15, 2024.