Genomic architecture of egg mimicry and its consequences for speciation in parasitic cuckoos

Host-parasite arms races facilitate rapid evolution and can fuel speciation. Cuculus cuckoos are deceptive egg mimics that exhibit a broad diversity of counterfeit egg phenotypes, representing host-adapted subpopulations (gentes). Genome analysis of 298 common ( Cuculus canorus ) and 50 oriental cuckoos ( Cuculus optatus ) spanning 15 egg morphs revealed that eggshell background coloration is predominantly influenced by matrilineal genetic variation. Recurrent mitochondrial mutations and an ancient W chromosome–linked translocation of an autosomal assembly factor for respiratory complex I provide a tentative link between mitochondrial function and pigment synthesis through the heme pathway. Biparentally inherited loci contribute to phenotypic variation in both species, mainly for maculation. The evolutionary tug-of-war over a sex-limited, mimetic trait integrates autosomal components with the nonrecombining, matrilineal genome without catalyzing genome-wide divergence between gentes.