Adaptive Evolution of Mitochondrial Energy Metabolism Genes Associated with Increased Energy Demand in Flying Insects

Insects are unique among invertebrates for their ability to fly, which raises intriguing questions about how energy metabolism in insects evolved and changed along with flight. Although physiological studies indicated that energy consumption differs between flying and non-flying insects, the evolution of molecular energy metabolism mechanisms in insects remains largely unexplored. Considering that about 95% of adenosine triphosphate (ATP) is supplied by mitochondria via oxidative phosphorylation, we examined 13 mitochondrial protein-encoding genes to test whether adaptive evolution of energy metabolism-related genes occurred in insects. The analyses demonstrated that mitochondrial DNA protein-encoding genes are subject to positive selection from the last common ancestor of Pterygota, which evolved primitive flight ability. Positive selection was also found in insects with flight ability, whereas no significant sign of selection was found in flightless insects where the wings had degenerated. In addition, significant positive selection was also identified in the last common ancestor of Neoptera, which changed its flight mode from direct to indirect. Interestingly, detection of more positively selected genes in indirect flight rather than direct flight insects suggested a stronger selective pressure in insects having higher energy consumption. In conclusion, mitochondrial protein-encoding genes involved in energy metabolism were targets of adaptive evolution in response to increased energy demands that arose during the evolution of flight ability in insects.昆虫作为无脊椎动物中唯一具备飞行能力的类群，其能量代谢如何随飞行演化而发生改变，这一问题引发了学界广泛的探究兴趣。尽管已有生理学研究证实飞行昆虫与非飞行昆虫的能量消耗存在差异，但目前学界对昆虫分子层面能量代谢机制的演化历程仍知之甚少。鉴于约95%的三磷酸腺苷（adenosine triphosphate，ATP）均由线粒体通过氧化磷酸化途径合成，本研究选取13个线粒体蛋白编码基因进行分析，以验证昆虫体内能量代谢相关基因是否发生了适应性演化。分析结果显示，线粒体DNA蛋白编码基因在具备原始飞行能力的有翅亚纲（Pterygota）最近共同祖先类群中便已受到正向选择作用。在具备飞行能力的昆虫类群中同样检测到了正向选择信号，而在翅膀退化的无翅昆虫类群中则未发现显著的选择痕迹。此外，在飞行模式从直接飞行转变为间接飞行的新翅亚纲（Neoptera）最近共同祖先类群中，同样检测到了显著的正向选择信号。值得注意的是，相较于直接飞行类昆虫，间接飞行类昆虫中检测到的正向选择基因数量更多，这提示能量消耗更高的昆虫类群承受了更强的选择压力。综上，参与能量代谢过程的线粒体蛋白编码基因，是昆虫在飞行能力演化过程中为适应能量需求提升而发生适应性演化的靶标基因。