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 can generate evolutionary conflict. Sex chromosomes may modulate these conflicts by biasing transmission of nuclear genes toward one sex. Here I synthesize theory and comparative evidence to propose that turnover in sex-determining systems, including 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 linked to non-recombining sex-linked regions, compensatory coevolution with maternally inherited mitochondria may be altered, potentially contributing to sex-biased incompatibilities. Subsequent turnover or recombination restoration may release these loci, reshaping the genomic context of conflict and generating cycles of amplification and relief. Evidence from animals, plants, and other systems highlights possible genomic and hybrid-zone signatures consistent with these dynamics, while also underscoring alternative mechanisms and important empirical gaps. Viewing sex chromosome turnover through the lens of cytonuclear interactions offers a framework for understanding how shifts in inheritance architecture may contribute to reproductive isolation, genomic divergence and, in some clades, diversification.