Hybridization drives mitochondrial DNA degeneration and metabolic shift in a species with biparental mitochondrial inheritance

Abstract

Mitochondrial DNA (mtDNA) is a cytoplasmic genome that is essential for respiratory metabolism. While uniparental maternal mtDNA inheritance is most common in animals and plants, distinct mtDNA haplotypes can coexist in a state of heteroplasmy, either because of paternal leakage or de novo mutations. MtDNA integrity and the resolution of heteroplasmy have important implications, notably for mitochondrial genetic disorders, genome evolution and speciation. However, knowledge on the factors driving heteroplasmy resolution is sparse. Here, we use Saccharomyces yeasts, fungi with constitutive biparental mtDNA inheritance, to investigate the resolution of mtDNA heteroplasmy in a variety of hybrid genotypes. We analyzed mtDNA sequence evolution and growth phenotypes in a collection of 864 hybrid yeast lines that were experimentally evolved under relaxed selection for mitochondrial function, allowing us to explore the near-neutral evolution of mtDNAs. The lines were subdivided into 11 different hybrid crosses among natural lineages of Saccharomyces paradoxus and its sister species Saccharomyces cerevisiae, yielding a variety of hybrid genotypes along a gradient of parental divergence. We observed extensive mtDNA recombination, but recombination rates were not predicted by parental divergence and were genotype-specific. However, we found a strong positive relationship between parental divergence and the rate of large-scale mtDNA deletions, which lead to the loss of respiratory metabolism. We also uncovered associations between mtDNA recombination, deletion, and genome instability that were genotype-specific. Our results show that hybridization in yeast induces mtDNA degeneration, with deep consequences for mtDNA evolution, metabolism and the emergence of reproductive isolation between species.

Evolution and maintenance of mtDNA gene content across eukaryotes

“…W. Taylor, 1986). Evidence seems mixed on whether recombination occurs readily over organismal (as opposed to evolutionary) timescales, with some studies observing extensive recombination (Hénault et al, 2022;Sena et al, 1986) and some with little observed (Y.-W. Wang et al, 2023). Of course, the observation of recombination will depend on many features including species and the extent of heteroplasmy (as in plants, above).…”