Maternal inheritance via the female-specific W chromosome was long ago proposed as a potential solution to the evolutionary enigma of co-existing host-specific races (or ‘gentes’) in avian brood parasites. Here we report the first unambiguous evidence for maternal inheritance of egg colouration in the brood-parasitic common cuckooCuculus canorus. Females laying blue eggs belong to an ancient (∼2.6 Myr) maternal lineage, as evidenced by both mitochondrial and W-linked DNA, but are indistinguishable at nuclear DNA from other common cuckoos. Hence, cuckoo host races with blue eggs are distinguished only by maternally inherited components of the genome, which maintain host-specific adaptation despite interbreeding among males and females reared by different hosts. A mitochondrial phylogeny suggests that blue eggs originated in Asia and then expanded westwards as female cuckoos laying blue eggs interbred with the existing European population, introducing an adaptive trait that expanded the range of potential hosts.

How cuckoos find the nests of their hosts and choose nests with respect to egg phenotype for parasitism is a long-standing puzzle that has so far not been solved. We recently developed an experimental design to shed light on this mystery by studying the egg-laying behavior of common cuckoos (Cuculus canorus) in nests of its Oriental reed warbler (Acrocephalus orientalis) host. Our results showed that common cuckoos only parasitized host nests with host activities but ignored the egg phenotypes in the nests. Furthermore, cuckoos distinguished between nest types of black-browed reed warbler (Acrocephalus bistrigiceps) and Oriential reed warbler and chose to parasitize the latter. This study provides strong evidence for host activities being a prime factor affecting cuckoo parasitism. Cuckoos must first locate the general site of host nests from activities by the host and then target the nests for parasitism. These observations reject the optimal egg-laying hypothesis stating that cuckoos are capable of choosing to lay eggs in host nests with visually matching egg phenotypes. Therefore, our studies challenge the idea that cuckoos recognize eggs that match their own.

Different populations of a host species subject to variable patterns of selection due to cuckoo parasitism provide an optimal situation for studying natural selection and coevolution in action. We compared egg appearance and egg-rejection behavior of 2 common cuckoo ( Cuculus canorus ) hosts, the ashy-throated parrotbill ( Paradoxornis alphonsianus ) and the vinous-throated parrotbill ( Paradoxornis webbianus ) between mainland China and Taiwan population that have been segregated for 2–3 million years. Avian visual modeling showed that the mainland host population under strong selection from brood parasitism has evolved polymorphic eggs, while the island host population released from brood parasitism has maintained the original monomorphic egg phenotype. Furthermore, experiments indicated that under such long historical segregation, egg rejection in the island population decayed dramatically in the absence of cuckoo parasitism. This study provides strong evidence that egg-rejection ability can be dramatically deficient in host populations without brood parasitism compared to parasitized ones. The results further enhance our understanding of changes in egg-rejection behavior in birds without the selection pressure of brood parasitism for an extended period of time.