Mitochondrial function in the evolutionary origin of the female germ line

Abstract

Oxidative phosphorylation couples ATP synthesis to respiratory electron transport. This coupling occurs in mitochondria, which carry DNA. Respiratory electron transport in the presence of molecular oxygen generates mutagenic reactive oxygen species (ROS) at a frequency that is itself increased by mutation. Damage to mitochondrial DNA (mtDNA) therefore accumulates within the lifespan of individual organisms. Syngamy requires motility of one gamete, and this motility requires ATP. It has been proposed that that oxidative phosphorylation is absent in the special case of quiescent, template mitochondria, and that these remain sequestered in oocytes and female germ lines. Oocyte mtDNA is thus protected from damage. Here I present evidence that female gametes, which are immotile, repress mitochondrial DNA transcription, mitochondrial membrane potential (!!m), and ROS production. In contrast, somatic cells and male gametes are seen actively to transcribe mitochondrial genes for respiratory electron carriers, and to produce ROS. I find that this functional division of labour between sperm and egg is widely distributed within the animal kingdom, and characterised by contrasting mitochondrial size and morphology. If quiescent oocyte mitochondria alone retain the capacity for an indefinite number of accurate replications of mtDNA, then "female" can be defined as that sex which transmits genetic template mitochondria. Template mitochondria then give rise to mitochondria that perform oxidative phosphorylation in somatic cells and in male gametes of each new generation. Template mitochondria also persist within the female germ line, to populate the oocytes of daughters. Thus mitochondria are maternally inherited.