The molecular evolutionary dynamics of oxidative phosphorylation (OXPHOS) genes in Hymenoptera

Shanlin Liu,Bernhard Misof,Jessica Ware,Oliver Niehuis,Yiyuan Li,Xin Zhou,Alexander Donath,Ralph S. Peters,Rui Zhang,Michael E. Pfrender

doi:10.1186/s12862-017-1111-z

Abstract

BackgroundThe 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.ResultsOur 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.ConclusionsOur 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.

Highlights

The primary energy-producing pathway in eukaryotic cells, the oxidative phosphorylation (OXPHOS) system, comprises proteins encoded by both mitochondrial and nuclear genes
The amino acid substitution rate among insect orders Using the sum of branch length between two species in the RAxML phylogenetic tree based on the concatenated sequence alignments as approximation for the amino acid substitution rate and using the two-cluster test in LINTREE [40], we found that Hymenoptera exhibited a higher amino acid substitution rate in both mitochondrial genes (Z statistics = 2.20, p-value
Hymenoptera exhibited a high amino acid substitution rate in their nuclear OXPHOS genes By comparing the amino acid sequences of OXPHOS genes of Hymenoptera to those of other holometabolous insects, we found that Hymenopterans exhibit a significantly elevated amino acid substitution rate in their mitochondrial and nuclear OXPHOS genes, but not in their nuclear non-OXHPOS genes (Fig. 2)

Summary

Introduction

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. Mitochondrial and nuclear OXPHOS genes work together to maintain the ATP production in the cell. As a result of the rapid rate of molecular evolution and accumulation of deleterious mutations in the mitochondrial genome, it has been suggested that that nuclear OXPHOS genes should be exposed to positive selection for compensatory substitutions that maintain the functional properties of the interacting genes in the OXPHOS system. As a result of the rapid rate of molecular evolution and accumulation of deleterious mutations in the mitochondrial genome, it has been suggested that that nuclear OXPHOS genes should be exposed to positive selection for compensatory substitutions that maintain the functional properties of the interacting genes in the OXPHOS system. [2, 6, 19,20,21]

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Results

Conclusion