Resetting the rules: Sex chromosome turnover as an escape hatch for mitonuclear conflict

Rachel L Moran 

Life’s diversity depends on both the stability and flexibility of inheritance systems. Mitochondrial and nuclear genomes must cooperate to sustain oxidative phosphorylation and cellular metabolism, yet their distinct inheritance routes often create conflict. Sex chromosomes modulate these conflicts by biasing transmission of thousands of nuclear genes toward one sex. Here I synthesize evidence that turnover in sex-determining systems, i.e., the gain, loss, or replacement of X, Y, Z, or W chromosomes, acts as an evolutionary “escape hatch’’ from persistent mitonuclear conflict. When nuclear-encoded mitochondrial (N-mt) genes become trapped in non-recombining sex-linked regions, coadaptation with maternally inherited mitochondria is constrained, producing sex-biased incompatibilities. Subsequent turnover can release these loci, resetting conflict intensity and creating pulses of hybrid breakdown and relief. Comparative data from plants, invertebrates, fishes, amphibians, birds, and mammals reveal predictable signatures of such cycles in genomes and hybrid zones. Viewing sex chromosome turnover through the lens of mitonuclear ecology links molecular evolution to macro-biodiversity: the same genomic resets that resolve conflict can also accelerate diversification.