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Evolutionary BiologybioRxiv
Preprint

Loss of the mitochondrial redox gene GLRX2 underlies somersaulting behavior in Darwin's pigeons

Si Si, Ling-Yan Su, Lan Long, You Qian, Wen-Di Ma, Xin Gan, Kun Jiang, Guo-Hao Wang, Zoltan Bagi, Daniele Bigi, Hamed Kharrati-Koopaee, Guang-Ze Zheng, Li MaiD, Zhuang Wu, Ming-Li Li, Hong-Man Chen, Qiu Pan, Wen-Jing Peng, Zhu Bu, Wen Gao, Jian Li, Ci-Rong Liu, Jia Pan, Jiu-Lin Du, Zhen Liu, , Ming-Shan Wang

Abstract

Darwin described the somersaulting behavior of pigeons as "one of the most remarkable inherited habits ever recorded", yet its molecular basis remained unknown. We show that somersaulting pigeon brains exhibit mitochondrial redox dysfunction and identify an 11-bp frameshifting deletion in GLRX2, a mitochondrial redox enzyme, that abolishes protein function and is highly-enriched in two independently selected breeds. GLRX2 deficiency in mice and zebrafish recapitulates mitochondrial dysfunction, oxidative stress and impaired motor coordination seen in pigeons. Single-nucleus transcriptomics identifies cerebellar Golgi and Purkinje cells as selectively vulnerable, with disrupted inhibitory signaling and synaptic remodeling. These findings demonstrate how relaxation of purifying selection during domestication can expose a deleterious mitochondrial variant to artificial selection, allowing gene loss to serve as a substrate for behavioral evolution.

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