Dietz Zachary P, Banerji Devshuvam, Sullins Jennifer A, Bever Brent W, Christy Stephen F, Bergthorsson Ulfar, Katju Vaishali, Estes Suzanne
Portland State University, Department of Biology, Portland, OR, USA.
Uppsala University, Department of Ecology and Genetics, Uppsala, Sweden.
Heredity (Edinb). 2025 Jul 28. doi: 10.1038/s41437-025-00786-6.
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.
几乎所有真核生物的代谢功能都依赖于由线粒体DNA（mtDNA）和核DNA（nDNA）基因组双重编码的分子机制。在进化过程中，这两个基因组保持了高度的协作，维持了包括氧化磷酸化和ATP产生在内的不可或缺的过程的能力，而这些过程反过来又影响许多与适应性相关的性状。当这一对基因组中的一个因有害突变而功能衰退时，这种协作是如何维持的，以及突变位置（mtDNA或nDNA）、交配系统或mtDNA拷贝数变化对这一过程的潜在补偿作用的影响，目前还知之甚少。我们研究了经历线粒体-核不匹配的群体是否以及在多大程度上能够通过让含有电子传递链（ETC）基因的线粒体或核突变的秀丽隐杆线虫在三种交配系统——兼性杂交（野生型）、专性自交和专性杂交——下进化60代来恢复到祖先的适应性水平。与进化理论一致，我们观察到适应性恢复的程度与菌株的祖先适应性水平之间呈反比关系，后者超过了交配系统的任何影响。我们根据之前报道的同一突变系中雄性频率的进化来解释这些发现。适应性进化量与mtDNA拷贝数变化之间的关系受到菌株的ETC突变背景及其与交配系统相互作用的影响。据我们所知，这项工作首次直接测试了生殖模式和线粒体-核不匹配下的进化对mtDNA基因组群体动态的影响。
