Selfish Mitonuclear Conflict

Abstract

Mitochondria, a nearly ubiquitous feature of eukaryotes, are derived from an ancient symbiosis. Despite billions of years of cooperative coevolution -in what is arguably the most important mutualism in the history of life -the persistence of mitochondrial genomes also creates conditions for genetic conflict with the nucleus. Because mitochondrial genomes are present in numerous copies per cell, they are subject to both within-and among-organism levels of selection. Accordingly, 'selfish' genotypes that increase their own proliferation can rise to high frequencies even if they decrease organismal fitness. It has been argued that uniparental (often maternal) inheritance of cytoplasmic genomes evolved to curtail such selfish replication by minimizing within-individual variation and, hence, within-individual selection. However, uniparental inheritance creates conditions for cytonuclear conflict over sex determination and sex ratio, as well as conditions for sexual antagonism when mitochondrial variants increase transmission by enhancing maternal fitness but have the side-effect of being harmful to males (i.e., 'mother's curse'). Here, we review recent advances in understanding selfish replication and sexual antagonism in the evolution of mitochondrial genomes and the mechanisms that suppress selfish interactions, drawing parallels and contrasts with other organelles (plastids) and bacterial endosymbionts that arose more recently. Although cytonuclear conflict is widespread across eukaryotes, it can be cryptic due to nuclear suppression, highly variable, and lineage-specific, reflecting the diverse biology of eukaryotes and the varying architectures of their cytoplasmic genomes.

Cytonuclear Genetic Incompatibilities in Plant Speciation

“…CMS is often the result of intergenomic conflict between the mitochondrial and the nuclear genomes [8,57,58]. Male-sterility mitochondrial genes will be selected as soon as they favor their own transmission via better seed production (their only way of transmission).…”

“…If, on the contrary, this first mutation is not neutral and impacts, for instance, possible interactions with other genes, these interactions might be re-established through positive selection. A third possibility is that BDMIs result from a genetic conflict between a selfish element that distorts segregation to increase its own transmission, inducing an arms-race to counteract its effect [5,7,8].…”

Selfish genes and sexual selection: the impact of genomic parasites on host reproduction

“…The uniparental inheritance of mitochondria, the powerhouse of cells, generates a conflict with the nuclear genome over sex determination and sex ratio, and also creates the opportunity for sexually antagonistic selection as mitochondria can increase maternal fitness but with a potential detrimental side effect to males – often referred to as ‘mothers curse’ (Gemmell, Metcalf & Allendorf, 2004; Havird et al , 2019). This occurs because mtDNA cannot evolve for male function as their heritability in males is zero.…”

Mitochondrial-nuclear coadaptation revealed through mtDNA replacements in Saccharomyces cerevisiae

“…While the coevolution of mitochondrial and nuclear genomes does occur, the unique biology of mitochondria complicates our view of a species' evolutionary history [32][33][34][35][36][37][38]. In most metazoans, uniparental inheritance, lack of recombination and high mutation rate of mtDNAs make it di cult to separate the effect of genetic drift from natural selection [39].…”