Effects of mating system and adaptedness on the evolution of fitness and mtDNA copy number in mitonuclear mismatched C. elegans.

Abstract

Metabolic functioning in nearly all eukaryotes relies on molecular machinery dual-encoded by mitochondrial DNA (mtDNA) and nuclear DNA (nDNA) genomes. The two genomes have sustained an extraordinary degree of cooperation across evolutionary time, preserving the capacity for indispensable processes including oxidative phosphorylation and ATP production, which in turn influence many fitness-related traits. How this cooperation is maintained when one member of the pair is debilitated by deleterious mutation is poorly understood, as is the influence of mutation location (mtDNA or nDNA), mating system, or the potentially compensatory effects of mtDNA copy number changes on the process. We asked whether and to what extent populations experiencing mitonuclear mismatch can recover ancestral levels of fitness by allowing C. elegans nematodes containing either mitochondrial or nuclear mutations of electron transport chain (ETC) genes to evolve under three mating systems-facultatively outcrossing (wildtype), obligately selfing, and obligately outcrossing-for 60 generations. In alignment with evolutionary theory, we observed an inverse relationship between the magnitude of fitness recovery and the ancestral fitness level of strains with the latter outweighing any effect of mating system. We interpret these findings in light of previously reported male frequency evolution in the same mutant lines. The relationship between the amount of fitness evolution and change in mtDNA copy number was influenced by strains' ETC mutant background and its interaction with mating system. To our knowledge, this work provides the first direct test of the effects of reproductive mode and evolution under mitonuclear mismatch on the population dynamics of mtDNA genomes.