Why are the mitochondria (the powerhouses of the cell) of male gametes destroyed shortly after fertilisation? Theory predicts that within-individual genomic conflict is the answer. Mitochondria contain independent genomes (mtDNA) and replicate independently of the cell cycle. If a cell contains multiple mitochondrial lineages we might expect mitochondria to be selected to replicate faster than other lineages in a biological ‘arms race’. While within-cell selection should favour mitochondrial lineages that replicate quickly, cell-level selection should prefer mitochondrial lineages with high metabolic activity. ‘Selfish’ mitochondria increase replication rate at a cost to metabolic activity and cell fitness, thereby creating a conflict between the mitochondrial and nuclear genomes. Uniparental inheritance is a nuclear-mediated mechanism that alleviates this theoretical conflict by preventing the mixing of, and competition between, different mitochondrial lineages. Destroying the mitochondria of male gametes is a common mechanism to ensure uniparental inheritance.
Although the above described ‘conflict theory’ seems plausible, the theory lacks experimental evidence. I will use the acellular slime mould Physarum polycephalum to test the basic assumptions of the conflict hypothesis. P. polycephalum is an excellent organism to empirically test this theory because nuclei and mitochondria replicate without cell division, creating an ideal environment for selection of selfish genomes. Moreover, crosses between specific P. polycephalum strains leads to biparental inheritance. The occurrence of both uniparental and biparental inheritance provides the opportunity to examine the fitness costs, if such costs exist, of the biparental inheritance of mitochondria.
My project has four aims. First, I will explore the regulation of mitochondrial inheritance in P. polycephalum. Second, I will develop a mathematical model to compare the theoretical costs of biparental versus uniparental inheritance in P. polycephalum. Third, I will experimentally assay the fitness of biparental and uniparental P. polycephalum strains across different life cycle stages. Finally, I will explore mechanisms that P. polycephalum may use to counteract the deleterious effects of these selfish organelles.