Ancient origin and maternal inheritance of blue cuckoo eggs.

Frode Fossøy,Eivin Røskaft,Michael D Sorenson,Anders P Møller,Fugo Takasu,Wei Liang,Arne Moksnes,Canchao Yang,Bård G Stokke,Jarkko Rutila,Torbjørn Ekrem

doi:10.1038/ncomms10272

Abstract

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 cuckoo Cuculus 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.

Highlights

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 in avian brood parasites
Population genetic analyses of pairwise genetic divergence revealed that cuckoos parasitizing redstarts in Finland, and laying immaculate blue eggs, were highly divergent from the other European host races in both their mitochondrial DNA and W chromosome DNA, but not at autosomal or Z-linked loci (MYO and SPIN—Fst range: 0.013–0.216, Fig. 2, Supplementary Table 2)
Our analyses of mitochondrial DNA (mtDNA) and W-linked DNA show that all common cuckoo females laying immaculate blue eggs belong to an ancient maternal lineage

Summary

Introduction

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. The first specific gene for egg colour in any bird species was recently discovered in the domestic chicken Gallus gallus, in which blue egg colour is associated with an autosomal, endogenous retroviral insertion, resulting in a dominant Mendelian trait[8]. We tested these alternative hypotheses with an expanded geographic sampling of common cuckoos (Fig. 1) and a particular focus on immaculate blue eggs, which are perhaps the most distinctive of all common cuckoo eggs (Fig. 2a)[9]. The blue egg colour is maternally inherited, supporting the hypothesis that the genes controlling egg colour are located on the female-specific W chromosome

Methods

Results

Conclusion