Comparative genomics reveals evolutionary signatures of genes underlying the ability to jump in beetles

Jumping is an effective strategy for arthropods to escape dangers, and has evolved independently in distinct lineages of beetles (order Coleoptera). Investigation of jumping behavior contributes to bionic applications and will deepen the understanding of adaptation and convergent evolution. However, regardless of extensive studies on jumping behavior of beetles, it remains unclear which and how genes have evolved underlying this locomotion mode. Here we performed comparative analysis of high-quality genomes, with one newly generated in this study, from jumping beetles (covering three families) and their non-jumping sister species spanning over 200 million years of evolution. We show that many genes involved in energy metabolism have experienced rapid evolution and/or positive selection in jumping beetles, reflecting the high energy-consuming nature of jumping activity. This observation, along with previous reports that genes associated with energy metabolism were involved in animal locomotion including flight, suggests shared molecular signatures across distinct locomotion modes. Moreover, we detected significant convergent evolution (convergent amino acid substitutions) in the leg disc development gene bab1, selection pressure and concurrently rapid evolution in dynein gene Dnai4, and significantly increased copy number of skeletal muscle gene Fhl2 in jumping beetles. Our results suggest that leg and muscle-related genes have played important roles in the evolution of beetle jumping. Overall, this study provides insights into genetic adaptation and convergent evolution of jumping behavior in beetles.