Accelerated sex chromosome degeneration and mitonuclear coevolution in a brood parasitic bird

The coevolution of interacting mitochondrial and nuclear genes involved in the oxidative phosphorylation (OXPHOS) pathway has received growing attention as a critical component of organismal fitness1 and potential source of genetic incompatibilities2–4 that promote speciation5–7. However, in species with “ZW” sex chromosomes, the mitochondrial genome and female-specific W chromosome are effectively linked by their shared matrilineal history, such that selection on either should subject both to the accumulation of deleterious mutations via genetic hitchhiking8,9. Thus, enhanced ecological selection on maternally inherited traits should accelerate both W chromosome degeneration and mitonuclear coevolution, though this prediction has not been tested empirically. Here we show that brood parasitic cuckoo finches Anomalospiza imberbis, in which mimetic egg coloration is maternally inherited, have experienced accelerated W chromosome pseudogenization and gene loss in addition to higher rates of amino acid substitution in both their mitochondrial and nuclear-encoded OXPHOS genes. Using a structural model of respiratory complex I, we also show that the degree of acceleration in nuclear-encoded residues is a function of their proximity to mtDNA-encoded residues, providing strong evidence of compensatory mitonuclear coevolution. Our results link ecological coevolution at the species level to both sex chromosome degeneration and mitonuclear coevolution, highlighting genomic consequences of selection on non-recombining genome components.