Optimal organelle inheritance strategies under different changing environments and mutational pressures

Abstract

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, oDNA is inherited and maintained by different classes of process. Inheritance is often maternal, but some species use paternal or doubly-uniparental (sex-dependent) inheritance (DUI), with different extents of “leakage” of oDNA from the non-primary parent. During development, genetic bottlenecks of different magnitudes and recombination-mediated repair are employed in different species. Here, we use modelling and simulation to investigate the fitness advantages, disadvantages, conflicts, and tradeoffs of these different strategies under different challenges of mutation and changes in selection imposed by the environment (in the absence of interactions with nuclear genes). We find a general tradeoff between maintaining heteroplasmy to support adaptation to environmental change, 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. We connect our findings to biologically observed behaviours, including the universality of non-minimal bottleneck sizes, a tradeoff between high ploidy for heteroplasmy and repair and tight bottlenecks for segregation, and environmental dependence of the benefits of leakage and DUI.