Optimal Organelle Inheritance Strategies Under Different Changing Environments and Mutational Pressures

Area of Science:

• Evolutionary biology
• Molecular genetics
• Cell biology

Background:

• Mitochondrial and chloroplast DNA (mtDNA and cpDNA) are crucial for cellular function and exist at high copy numbers (ploidy).
• Organelle DNA (oDNA) maintenance requires balancing mutation mitigation with adaptation to environmental demands.
• Eukaryotic oDNA inheritance varies (maternal, paternal, doubly-uniparental inheritance [DUI]) with differing parental leakage, alongside developmental bottlenecks and repair mechanisms.

Purpose of the Study:

• To investigate the fitness consequences of different oDNA inheritance and maintenance strategies.
• To explore tradeoffs between adaptation and purifying selection under varying environmental and mutational pressures.
• To model the impact of leakage and bottleneck size on oDNA dynamics in the absence of nuclear gene interactions.

Main Methods:

• Utilized mathematical modeling and computer simulations.
• Investigated various scenarios of mutation rates and environmental selection changes.
• Analyzed the effects of different leakage extents and bottleneck sizes.

Main Results:

• Identified a fundamental tradeoff between maintaining heteroplasmy for adaptation and purifying selection against deleterious mutants.
• Demonstrated that specific combinations of leakage and bottleneck size optimize oDNA strategies under distinct challenges.
• Found that non-minimal bottleneck sizes are universally observed, reflecting a balance between repair/ploidy and segregation.

Conclusions:

• oDNA inheritance and maintenance strategies are shaped by evolutionary tradeoffs.
• The optimal strategy for oDNA management is context-dependent, influenced by environmental factors and mutation rates.
• Observed biological behaviors, such as DUI and bottleneck sizes, align with model predictions regarding adaptation and mutation control.