Paternal leakage of organelles can improve adaptation to changing environments

Sexual eukaryotes have diverse mechanisms preventing the biparental inheritance of mitochondria and plastids, and reducing the coexistence of dissimilar organelle DNA (heteroplasmy). Nevertheless, paternal leakage often occurs in plants, fungi, protists and animals, and this leaves the possibility that heteroplasmy can in some contexts be advantageous. Theoretical models developed in the past revealed that maternal inheritance improves selection against deleterious mitochondrial mutations, but none of them have explained the observed variation in the extent of paternal leakage. Here we show that paternal leakage regulated by nuclear loci can evolve to maintain advantageous organelle diversity in fluctuating environments. Strict maternal inheritance reduces organelle variance within the cell, but this loss of diversity can be detrimental when environments are shifting rapidly. Our model reveals that high levels of paternal leakage can evolve in these types of rapidly changing environments and that strict maternal inheritance evolves only when the environment is changing slowly.