Comparative genomics reveals evolutionary signatures of genes associated with jumping in beetles
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Wei Wang,
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Le Zong,
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Jin-Wu He,
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Chu-Yang Mao,
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Zhi-Wei Dong,
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Ping-Ping Yang,
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Zheng-Zhong Huang,
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Cong-Qiao Li,
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Wen-Jie Li,
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Yong-Ying Ruan,
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Chuan Feng,
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Xue-Yan Li,
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Si-Qin Ge
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Abstract
Jumping has independently emerged as an effective escape strategy across multiple beetle lineages (order Coleoptera). Characterization of jumping behavior not only informs the development of bioinspired robotic systems but also advances understanding of adaptive processes and convergent evolution. However, despite extensive behavioral studies in beetles, the genetic mechanisms and evolutionary trajectories underlying this locomotor strategy remain largely unresolved. To elucidate the molecular basis of jumping adaptation and convergent evolution, a comparative genomic analysis was conducted using high-quality assemblies, including one newly generated genome, from jumping beetles representing three families and their non-jumping sister taxa spanning over 200 million years of evolutionary divergence. Genes associated with energy metabolism exhibited extensive signals of rapid evolution and positive selection in jumping beetles, consistent with the elevated energy requirements of explosive locomotion. These observations parallel previous reports linking energy metabolism genes to other high-demand locomotor modes such as flight, suggesting shared molecular signatures across functionally distinct behaviors. Jumping beetles exhibited convergent amino acid substitutions in bab1, a regulator of leg disc development, alongside evidence of positive selection and accelerated evolution in the dynein gene Dnai4 and a significant expansion in copy number of the skeletal muscle gene Fhl2. Together, these results implicate both limb morphogenesis and muscle performance genes in the emergence of beetle jumping. This study highlights key genetic mechanisms underlying behavioral innovation and offers novel insights into adaptive convergence in insect locomotion.
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