Maternal inheritance accelerates sex chromosome degeneration and mitonuclear coevolution in a brood parasitic bird

The coevolution of interacting mitochondrial and nuclear genes is increasingly recognized as a critical component of organismal fitness and a potential source of genetic incompatibilities that promote speciation. In species with 'ZW' sex chromosomes, however, selection on maternally inherited traits may impact mitonuclear coevolution owing to the effective linkage of the W chromosome and mitochondrial DNA (mtDNA). Here we show that in brood parasitic cuckoo finches (Anomalospiza imberbis), enhanced ecological selection on a maternally inherited trait (mimetic egg colouration) subjects both the W chromosome and mtDNA to increased accumulation of slightly deleterious mutations via genetic hitchhiking, accelerating W chromosome pseudogenization and gene loss, as well as mitonuclear coevolution. Remarkably, as other W-linked genes were lost, two egg colour genes, representing likely targets of selection during cuckoo finch-host coevolution, were recruited to the W chromosome. Using structural models of the respiratory complexes and mitoribosome, we also show that the rate of amino acid substitution in nuclear-encoded residues is a function of their proximity to mtDNA-encoded residues, providing evidence of compensatory mitonuclear coevolution. Our results link species-level coevolution to both sex chromosome degeneration and mitonuclear coevolution. More generally, they highlight the genomic consequences of adaptation without recombination.