title: 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.
authors.affiliation: Deptartment of Biological Sciences, Auburn University, Auburn, AL, USA.|Department of Biology, Colorado State University, Fort Collins, CO, USA.
authors.forename: Justin C
authors.initials: JC
authors.lastname: Havird
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Matthew D
authors.initials: MD
authors.lastname: Hall
authors.affiliation: School of Biological Sciences, Monash University, Victoria, Australia.
authors.forename: Damian K
authors.initials: DK
authors.lastname: Dowling
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics; D000818:Animals; D005075:Biological Evolution; D002467:Cell Nucleus / Q000235:genetics; D056890:Eukaryota / Q000235:genetics*; D006801:Humans; D008928:Mitochondria / Q000235:genetics*; D008954:Models, Biological; D009154:Mutation / Q000235:genetics*; D011995:Recombination, Genetic; D012727:Sex Characteristics
keywords: cytonuclear; evolutionary genomics; mito-mutation accumulation; mito-nuclear interactions; mitochondrial replacement; organelle; recombination