Flight style and metabolism shape the tempo of genome evolution in birds

by Yanzhu Ji, Lei Wu, Dongming Li, Shaohong Feng, Qi Fang, Ying Xiong, Yongbin Chang, Jacob C. Cooper, Xin Yu, Kai Zhang, Shiyu Tang, Huishang She, Huan Wang, Dezhi Zhang, Gang Song, Ping Fan, Jiaogen Zhou, Liang Ma, Yanhua Qu, Chenxi Jia, Catherine Sheard, James Andrew DeWoody, Joseph A. Tobias, Guojie Zhang, Weiwei Zhai, Fumin Lei

As a hallmark of avian ecological innovation, powered flight has fundamentally shaped diverse aspects of birds. The energy demand of flight may have mutagenic impacts on genomes, influencing how fast genomes evolve. However, the relationship between flight, metabolism, and evolutionary rates remains relatively underexplored. Leveraging 363 newly available avian genomes from >90% of avian families, we quantified three distinct types of genomic evolutionary rates to capture a broad spectrum of mutational processes. By combining four flight-related traits and three metabolic metrics, we uncovered significant associations between flight style, metabolism, and multiple evolutionary rates. Next, using a causal inference framework, we demonstrated that metabolism accounted for 43.3% of the total effect between flight and evolutionary rate, underscoring its key role. Together, our findings establish a robust connection between flight, metabolism, and evolutionary rates, offering new insights into how key innovations and associated phenotypes shape the tempo of genome evolution.