Virulence of avian brood parasites can trigger a coevolutionary arms race, which favours rejection of parasitic eggs or chicks by host parents, and in turn leads to mimicry in parasite eggs or chicks [1-7]. The appearance of host offspring is critical to enable host parents to detect parasites. Thus, increasing accuracy of parasites' mimicry can favour a newly emerged host morph to escape parasites' mimicry. If parasites catch up with the hosts with a newly acquired mimetic morph, host polymorphism should be maintained through apostatic (negative frequency-dependent) selection, which favours hosts rarer morphs [1-3,7]. Among population-wide polymorphism, uniformity of respective host morphs in single host nests stochastically prevents parasites from targeting any specific morph of hosts and thus helps parents detect parasitism. Polymorphism in such a state is well-known in egg appearances of hosts of brood parasitic birds [2,3,7], which might also occur in chick appearances when arms races escalate. Here, we present evidence of polymorphism in chick skin coloration in a cuckoo-host system: the fan-tailed gerygone Gerygone flavolateralis and its specialist brood parasite, the shining bronze-cuckoo Chalcites lucidus in New Caledonia (Figure 1A-C).

Mimicry by avian brood parasites favours uniformity over variation within a breeding attempt as host defence against parasitism. In a cuckoo-host system from New Caledonia, the arms race resulted in both host (Gerygone flavolateralis) and parasite (Chalcites lucidus) having nestlings of two discrete skin colour phenotypes, bright and dark. In our study sites, host nestlings occurred in monomorphic and polymorphic broods, whereas cuckoo nestlings only occurred in the bright morph. Irrespective of their brood colour, host parents recognised and ejected parasite nestlings but never ejected their own. We investigated whether host parents visually recognised their own nestlings by using colour, luminance and pattern of multiple body regions. We found that the parasite mimicked multiple visual features of both host morphs and that the visual difference between host morphs was larger than the difference between the parasite and the mimicked host morph. Visual discrimination alone may result in higher chances of recognition errors in polymorphic than in monomorphic host broods. Host parents may rely on additional sensorial cues, not only visual, to assess nestling identity. Nestling polymorphism may be a trace of evolutionary past and may only have a marginal role in true-recognition of nestlings in the arms race in New Caledonia.

Apart from a few well-studied examples, there is little information regarding the life history and ecological requirements of brood parasites and their hosts in most cuckoo-host systems, particularly in tropical areas. In New Caledonia, the Fan-tailed Gerygone Gerygone flavolateralis, is the exclusive host of the Shining Bronze-cuckoo, Chalcites lucidus. Here, the arms race has escalated to the nestling stage, and both host and parasite have polymorphic (difference in skin coloration) nestlings. This is a novel system for the study of brood parasitism, but very little is known about the breeding biology of the Fan-tailed Gerygone and how this may affect the co-evolutionary interactions with the Shining Bronze-cuckoo. We monitored active nests of the Fan-tailed Gerygone during six breeding seasons, using video monitoring and direct observation. Nest attendance periods of host parents were shorter during laying than during incubation, and therefore parasitism was more likely to occur during the laying period. Cuckoos eggs were on average 2 days more developed than host eggs, and thus cuckoo nestlings usually hatched before host nestlings. Fan-tailed Gerygone nestling phenotypes had similar growth and fledging rates and their frequency did not differ between habitats, indicating no apparent trade-off with skin coloration. The precipitation regime affected predation but not the parasitism rate. The current situation in New Caledonia suggests a higher selection pressure on the parasite than on the host. Our study highlights the importance of data on the breeding biology of the host in the context of studies on brood parasitism. Keywords Arms race • Nestling polymorphism • Laying synchrony • Frontline defences • Cuckoo chick ejection Zusammenfassung Brutbiologie der Fächerschwanzgerygone Gerygone flavolateralis unter Berücksichtigung der Parasitierung durch den Bronzekuckuck Chalcites lucidus Abgesehen von wenigen gut untersuchten Beispielen zum koevolutionären Wettrüsten zwischen Brutparasiten und Wirten gibt es, insbesondere in tropischen Gebieten, nur geringe Kenntnisse zur Lebensweise und zu den ökologischen Anforderungen von Kuckucken und deren Wirten. In Neukaledonien ist die Fächerschwanzgerygone, Gerygone flavolateralis, der einzige Wirt des Bronzekuckucks, Chalcites lucidus. Auf dieser Insel hat sich das Wettrüsten auf die Kükenphase ausgeweitet und sowohl Wirt als auch Parasit haben polymorphe Küken (Unterschiede in der Hautfärbung). Dies eröffnet neue Möglichkeiten für das Studium von Brutparasitismus. Es ist jedoch sehr wenig über die Brutbiologie der Fächerschwanzgerygone und die möglichen koevolutionären Wechselwirkungen mit dem Bronzekuckuck bekannt. Wir haben aktive Nester der Fächerschwanzgerygone über sechs Brutzeiten mit Videokameras und direkten Beobachtungen Communicated by F. Bairlein.

Nestling ejection is a rare type of host defence against brood parasitism compared to egg ejection. Theoretically, host defences at both egg and nestling stages could be based on similar underlying discrimination mechanisms but, due to the rarity of nestling ejector hosts, few studies have actually tested this hypothesis. We investigated egg and nestling discrimination by the fan-tailed gerygone Gerygone flavolateralis, a host that seemingly accepts non-mimetic eggs of its parasite, the shining bronze-cuckoo Chalcites lucidus, but ejects mimetic parasite nestlings. We introduced artificial eggs or nestlings and foreign gerygone nestlings in gerygone nests and compared begging calls of parasite and host nestlings. We found that the gerygone ejected artificial eggs only if their size was smaller than the parasite or host eggs. Ejection of artificial nestlings did not depend on whether their colour matched that of the brood. The frequency of ejection increased during the course of the breeding season mirroring the increase in ejection frequency of parasite nestlings by the host. Cross-fostered gerygone nestlings were frequently ejected when lacking natal down and when introduced in the nest before hatching of the foster brood, but only occasionally when they did not match the colour of the foster brood. Begging calls differed significantly between parasite and host nestlings throughout the nestling period. Our results suggest that the fan-tailed gerygone accepts eggs within the size range of gerygone or cuckoo eggs and that nestling discrimination is based on auditory and visual cues other than skin colour. This highlights the importance of using a combined approach to study discrimination mechanisms of hosts.

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