Positive Selection Drove the Adaptation of Mitochondrial Genes to the Demands of Flight and High-Altitude Environments in Grasshoppers.

Xiao-Dong Li,Ran Li,Wei-An Deng,Li-Yun Yan,Guo-Fang Jiang,Yuan Mu

doi:10.3389/fgene.2018.00605

Xiao-Dong Li, Ran Li + Show 4 more

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https://doi.org/10.3389/fgene.2018.00605

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Abstract

The molecular evolution of mitochondrial genes responds to changes in energy requirements and to high altitude adaptation in animals, but this has not been fully explored in invertebrates. The evolution of atmospheric oxygen content from high to low necessarily affects the energy requirements of insect movement. We examined 13 mitochondrial protein-coding genes (PCGs) of grasshoppers to test whether the adaptive evolution of genes involved in energy metabolism occurs in changes in atmospheric oxygen content and high altitude adaptation. Our molecular evolutionary analysis of the 13 PCGs in 15 species of flying grasshoppers and 13 related flightless grasshoppers indicated that, similar to previous studies, flightless grasshoppers have experienced relaxed selection. We found evidence of significant positive selection in the genes ATP8, COX3, ND2, ND4, ND4L, ND5, and ND6 in flying lineages. This results suggested that episodic positive selection allowed the mitochondrial genes of flying grasshoppers to adapt to increased energy demands during the continuous reduction of atmospheric oxygen content. Our analysis of five grasshopper endemic to the Tibetan Plateau and 13 non-Tibetan grasshoppers indicated that, due to positive selection, more non-synonymous nucleotide substitutions accumulated in Tibetan grasshoppers than in non-Tibetan grasshoppers. We also found evidence for significant positive selection in the genes ATP6, ND2, ND3, ND4, and ND5 in Tibetan lineages. Our results thus strongly suggest that, in grasshoppers, positive selection drives mitochondrial genes to better adapt both to the energy requirements of flight and to the high altitude of the Tibetan Plateau.

Highlights

Adenosine triphosphate (ATP) directly provides the free energy needed for animal locomotion (Shen et al, 2009)
The relaxed selection was associated with flight loss of insects (Mitterboeck and Adamowicz, 2013; Mitterboeck et al, 2017); and significant positive selection was shown on the mitochondrial proteincoding genes (PCGs) of the most recent common ancestor of Pterygota, as well as on the mitochondrial PCGs of flying insects (Yang et al, 2014; Mitterboeck et al, 2017)
Considering that there is a proportional relationship between the amount of ATP produced by animals and the concentration of oxygen in a certain range, animals need more efficient energy metabolism when locomoting in a low oxygen environment

Summary

Introduction

Adenosine triphosphate (ATP) directly provides the free energy needed for animal locomotion (Shen et al, 2009). Mitochondrial genes are key to the evolution of the cellular mechanisms that metabolize molecular energy (Da et al, 2008). Mitochondrial genes were even targets of natural selection and allowed adaptation to the huge change in energy demand that were required during the origin of bat flight (Shen et al, 2010). The recent high peak (32%) of atmospheric oxygen content is about 100 million years ago (Bergman et al, 2004). We speculate that in the evolution of high-oxygen environments to lowoxygen environments, in order to maintain flight capability of insects, more efficient energy metabolism mechanisms are needed. That genes involved in energy metabolism allowed adaptation to the huge change in energy demand

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