The evolution of sex: A new hypothesis based on mitochondrial mutational erosion: Mitochondrial mutational erosion in ancestral eukaryotes would favor the evolution of sex, harnessing nuclear recombination to optimize compensatory nuclear coadaptation

Abstract

The evolution of sex in eukaryotes represents a paradox, given the "twofold" fitness cost it incurs. We hypothesize that the mutational dynamics of the mitochondrial genome would have favored the evolution of sexual reproduction. Mitochondrial DNA (mtDNA) exhibits a high-mutation rate across most eukaryote taxa, and several lines of evidence suggest that this high rate is an ancestral character. This seems inexplicable given that 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.

Keywords: cytonuclear; evolutionary genomics; mito-mutation accumulation; mito-nuclear interactions; mitochondrial replacement; organelle; recombination.

Figure 1

Mutational meltdown in the mitochondrial DNA (mtDNA) is offset by compensatory changes in the nuclear DNA, facilitated by recombination associated with sexual reproduction, providing a mechanism for the origin and maintenance of sexual reproduction. “Mutation load” is displayed on the y-axis and denotes total number of deleterious mutations. Even though the absolute number of mutations in the mitochondrial genome remains the same in panel (a) and (b), in (b) the deleterious effects of mito-mutations are offset by nuclear compensatory adaptations in the recombined nuclear genome (hence, the mutation load is lower under sexual reproduction). A: During asexual reproduction, mito-nuclear mismatch increases over generations as mtDNA accumulates mutations faster than the nuclear genome can evolve counter-adaptations. B: With sexual reproduction, organismal viability is restored in the population by selection for compensatory genotypes in the nucDNA, facilitated by recombination. Orange/dotted lines represent mtDNA, blue/solid lines represent nucDNA, and dashed lines represent a fatal upper threshold for mito-nuclear mismatch.

Figure 2

A model for early eukaryotic evolution. Under our hypothesis, the evolution of recombination via sexual reproduction stems from the need to shuffle nuclear genes, as an inevitable consequence of having mitochondria. We envisage that this was driven by high mtDNA mutation rates in the early endosymbiotic bacterium that evolved into the mitochondrion. Following acquisition of the bacterial endosymbiont, the early eukaryote would have transmitted its endosymbiont vertically (number 1), without recombination, leading to mutational erosion in the mtDNA. Numbers indicate the general temporal order of other events, including the evolution of sex, based on our hypothesis. Lightning bolts denote DNA mutations, orange/blue denotes mtDNA and nuclear DNA, respectively, and different shading represents DNA from different lineages. Circles denote host nucleus and associated genome, and the eclipses denote mitochondria and their mtDNA.