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. <i>Cuculus</i> cuckoos are deceptive egg mimics that exhibit a broad diversity of counterfeit egg phenotypes, representing host-adapted subpopulations (gentes). Genome analysis of 298 common (<i>Cuculus canorus</i>) and 50 oriental cuckoos (<i>Cuculus optatus</i>) 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.