Justin Havird , Matthew D Hall , Damian Dowling
The evolution of sex in eukaryotes represents a paradox, given the “two-fold” fitness cost it incurs. We hypothesize that the mutational dynamics of the mitochondrial genome would have favoured the evolution of sexual reproduction. Mitochondrial DNA (mtDNA) exhibits a high mutation rate across most eukaryote taxa, and several lines of evidence suggest this high rate is an ancestral character. This seems inexplicable given mtDNA-encoded genes underlie the expression of life’s most salient functions, including energy conversion. We propose that negative metabolic effects linked to mitochondrial mutation accumulation would have invoked selection for sexual recombination between divergent host nuclear genomes in early eukaryote lineages. This would provide a mechanism by which recombinant host genotypes could be rapidly shuffled and screened for the presence of compensatory modifiers that offset mtDNA-induced harm. Under this hypothesis, recombination provides the genetic variation necessary for compensatory nuclear coadaptation to keep pace with mitochondrial mutation accumulation.