Gatekeepers of the Germ Line: How Mitochondria Shape Reproductive Evolution in Metazoans

Mitochondria play essential roles for animal reproduction, influencing not only cellular energetics but also gamete quality, inheritance and evolutionary patterns. Currently, most research still focuses on chordates or mitochondrial diseases and their impact on the health of germ cells. However, few studies focus on integrative synthesis that connect comparative morphology, inheritance mechanisms and evolutionary theory. In this review, we integrate cross-phyla evidence to explore two interconnected dimensions: the fate of mitochondria during gametogenesis and the strategy shaping their evolution. We compare mitochondrial morphology, distribution, and metabolic strategies in gametogenesis, revealing how these traits align with reproductive modes and ecological adaptations. Then we further discuss how mitochondrial genome evolution, bottleneck effects and mito-nuclear coevolution contribute to germline stability and maternal inheritance. Special attention is given to exceptional systems such as Doubly Uniparental Inheritance (DUI) in bivalves, which challenges conventional mode of strictly maternal transmission and illuminates the flexibility of mito-nuclear evolution. Altogether, these perspectives highlight mitochondria as gatekeepers and evolutionary recorders in the reproductive systems across metazoans, providing a unifying framework for future research across ecology, evolution and molecular biology.