Department of Mathematics, University of Bergen, Bergen, Norway.
Charles Perkins Centre, University of Sydney, Sydney, NSW, Australia.
J Evol Biol. 2021 May;34(5):757-766. doi: 10.1111/jeb.13776. Epub 2021 May 11.
Across eukaryotes, genes encoding bioenergetic machinery are located in both mitochondrial and nuclear DNA, and incompatibilities between the two genomes can be devastating. Mitochondria are often inherited maternally, and theory predicts sex-specific fitness effects of mitochondrial mutational diversity. Yet how evolution acts on linkage patterns between mitochondrial and nuclear genomes is poorly understood. Using novel mito-nuclear population-genetic models, we show that the interplay between nuclear and mitochondrial genes maintains mitochondrial haplotype diversity within populations, and selects both for sex-independent segregation of mitochondrion-interacting genes and for paternal leakage. These effects of genetic linkage evolution can eliminate male-harming fitness effects of mtDNA mutational diversity. With maternal mitochondrial inheritance, females maintain a tight mitochondrial-nuclear match, but males accumulate mismatch mutations because of the weak statistical associations between the two genomic components. Sex-independent segregation of mitochondria-interacting loci improves the mito-nuclear match. In a sexually antagonistic evolutionary process, male nuclear alleles evolve to increase the rate of recombination, whereas females evolve to suppress it. Paternal leakage of mitochondria can evolve as an alternative mechanism to improve the mito-nuclear linkage. Our modelling framework provides an evolutionary explanation for the observed paucity of mitochondrion-interacting genes on mammalian sex chromosomes and for paternal leakage in protists, plants, fungi and some animals.
在真核生物中，编码生物能量机制的基因位于线粒体和核 DNA 中，两个基因组之间的不兼容性可能是毁灭性的。线粒体通常通过母系遗传，理论预测线粒体突变多样性对性别特异性适应度有影响。然而，进化对线粒体和核基因组之间的连锁模式的作用方式还了解甚少。使用新的线粒体-核群体遗传模型，我们表明，核基因和线粒体基因之间的相互作用维持了种群内线粒体单倍型多样性，并选择了与线粒体相互作用基因的非性别独立分离以及父系渗漏。遗传连锁进化的这些影响可以消除 mtDNA 突变多样性对男性有害的适应度影响。由于两个基因组成分之间的统计关联较弱，在母系线粒体遗传中，女性保持着紧密的线粒体-核匹配，但男性会积累不匹配的突变。线粒体相互作用基因的非性别独立分离可以改善线粒体-核匹配。在一个性拮抗的进化过程中，雄性核等位基因进化以增加重组率，而雌性则进化以抑制重组。线粒体的父系渗漏可以作为改善线粒体-核连锁的替代机制而进化。我们的模型框架为观察到的哺乳动物性染色体上的线粒体相互作用基因数量较少以及原生动物、植物、真菌和一些动物中的父系渗漏提供了进化解释。
