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Evolutionary dynamics of OXPHOS genes in Hymenoptera

Mitochondrion is the major energy production organelle in eukaryotes, generating more than 70% of the ATPs through the OXPHOS pathway, which consists of proteins encoded by both mitochondrial and nuclear genes. We investigated nucleotide substitution rates and selective pressures for OXPHOS genes of the 4 major insect orders. The results show that hymenopterans have the highest substation rates in mitochondrial OXPHOS genes and substantially elevated rates in their nuclear OXPHOS genes. Although positive selection has been identified in some of these nuclear OXPHOS genes, other evolutionary drivers may also play important roles in the fast molecular evolution pattern in hymenopterans.

Li, Y., R. Zhang, S. Liu, A. Donath, R. S. Peters, J. Ware, B. Misof, O. Niehuis, M. E. Pfrender*, and X. Zhou*. 2017. The molecular evolutionary dynamics of Oxidative Phosphorylation (OXPHOS) genes in Hymenoptera. BMC Evolutionary Biology 17:269. PDF


Background: The primary energy-producing pathway in eukaryotic cells, the oxidative phosphorylation (OXPHOS) system, comprises proteins encoded by both mitochondrial and nuclear genes. To maintain the function of the OXPHOS system, the pattern of substitutions in mitochondrial and nuclear genes may not be completely independent. It has been suggested that slightly deleterious substitutions in mitochondrial genes are compensated by substitutions in the interacting nuclear genes due to positive selection. Among the four largest insect orders, Coleoptera (beetles), Hymenoptera (sawflies, wasps, ants, and bees), Diptera (midges, mosquitoes, and flies) and Lepidoptera (moths and butterflies), the mitochondrial genes of Hymenoptera exhibit an exceptionally high amino acid substitution rate while the evolution of nuclear OXPHOS genes is largely unknown. Therefore, Hymenoptera is an excellent model group for testing the hypothesis of positive selection driving the substitution rate of nuclear OXPHOS genes. In this study, we report the evolutionary rate of OXPHOS genes in Hymenoptera and test for evidence of positive selection in nuclear OXPHOS genes of Hymenoptera.

Results: Our analyses revealed that the amino acid substitution rate of mitochondrial and nuclear OXPHOS genes in Hymenoptera is higher than that in other studied insect orders. In contrast, the amino acid substitution rate of non-OXPHOS genes in Hymenoptera is lower than the rate in other insect orders. Overall, we found the dN/dS ratio of the nuclear OXPHOS genes to be higher in Hymenoptera than in other insect orders. However, nuclear OXPHOS genes with high dN/dS ratio did not always exhibit a high amino acid substitution rate. Using branch-site and site model tests, we identified various codon sites that evolved under positive selection in nuclear OXPHOS genes.

Conclusions: Our results showed that nuclear OXPHOS genes in Hymenoptera are evolving faster than the genes in other three insect orders. The branch test suggested that while some nuclear OXPHOS genes in Hymenoptera show a signature of positive selection, the pattern is not consistent across all nuclear OXPHOS genes. As only few codon sites were under positive selection, we suggested that positive selection might not be the only factor contributing to the rapid evolution of nuclear OXPHOS genes in Hymenoptera.

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