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

Abstract

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.