Optimal organelle inheritance strategies under different changing environments and mutational pressures

Mitochondrial and chloroplast DNA (mtDNA and cpDNA) encode essential cellular apparatus. This organelle DNA (oDNA) exists at high copy number (ploidy) in eukaryotic cells, which must both mitigate mutational damage and allow adaptation to changing demands. Across eukaryotes, a range of inheritance strategies are used for oDNA, including uniparental and doubly uniparental inheritance (DUI), paternal leakage, recombination-mediated repair and gene conversion, and an effective “genetic bottleneck” imposed between generations. Here, we use modelling and simulation to investigate how these different strategies support the robustness and evolvability of oDNA populations under different challenges of mutation and changes in selection imposed by the environment. We find a general tradeoff between maintaining heterozygosity for flexible adaptation and supporting purifying selection against dysfunctional mutants. Different combinations of leakage and bottleneck size provide optimal resolutions to this tradeoff under different sets of challenges. The model explains many observed behaviours, including the appearance of non-minimal bottleneck sizes, a tradeoff between high ploidy for heterozygosity and repair and tight bottlenecks for segregation, and environmental dependence of the benefits of leakage and DUI. We connect different strategies observed across eukaryotes with the ecology of the organisms involved to explore support for the predictions of this theory.