Nestling polymorphism in a cuckoo-host system

Abstract

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).

True recognition of nestlings by hosts selects for mimetic cuckoo chicks

“…Despite typically suffering high parasitism rates, gerygones do not reject bronze-cuckoo eggs [13,14,17]. Instead, gerygones have the most effective known form of chick rejection because they reject cuckoo chicks by dragging them out of the nest within hours of hatching [13,14,18], sometimes succeeding in removing the cuckoo nestling (a nest-mate evictor) before it has a chance to evict the host young from the nest. Most Australian bronze-cuckoo species lay non-mimetic eggs, but their chicks are excellent visual mimics of host young, with each subspecies matching the colour of nestling skin, rictal flange and down-feathers of their favoured host species [15,19,20].…”

Impact of brood parasitism and predation on nest survival of the fan‐tailed gerygone in New Caledonia

“…In turn, this defence by the host promoted mimicry by the cuckoo nestling (Attisano et al ) similar to other bronze‐cuckoo species from Australia (Sato et al , Langmore et al ). In addition, nestlings of both hosts and parasites occur in two skin colour morphs, bright and dark (Sato et al ). This system evolved in the absence of humans and mammalian predators, but the arrival of humans may have changed the ecological conditions.…”

Breeding biology of the Fan-tailed Gerygone Gerygone flavolateralis in relation to parasitism by the Shining Bronze-cuckoo Chalcites lucidus

“…Frontline defences (Feeney et al 2012) are present at least in the Grey Warbler, Gerygone igata, which seems to recognise and attack bronze-cuckoos approaching the nest (Briskie 2007), but it is unknown if this occurs in other Gerygone species or if frontline defences extend to nest surveillance as in other bronze-cuckoo hosts (Feeney and Langmore 2015). Gerygone species do not seem to be able to reject cuckoo eggs (Mulyani 2004;Langmore et al 2005Langmore et al , 2009Gloag et al 2014;Thorogood et al 2017), but can discriminate and eject the parasite nestling from the nest (Sato et al 2010a(Sato et al , 2015Tokue and Ueda 2010). This host defence strategy has been reported for the Large-billed Gerygone, G. magnirostris (Sato et al 2010a), and the Mangrove Gerygone, G. laevigaster (Tokue and Ueda 2010), from Australia, which are parasitised by the Little Bronze-cuckoo, Chalcites minutillus, and in the Fantailed Gerygone, G. flavolateralis (Sato et al 2015;Attisano et al 2018), which is parasitised by the local subspecies of the Shining Bronze-cuckoo, Chalcites lucidus layardi, in New Caledonia.…”

“…Other hosts of brood parasites can discriminate the parasite nestling (Langmore et al 2003) or fledgling (Grim 2007), but they do so only after the loss of their entire clutch or brood. Gerygone hosts, in contrast, discriminate the parasite nestling before it can evict host eggs or nestlings (Sato et al 2010a(Sato et al , 2015Tokue and Ueda 2010;Attisano et al 2018) and thus save their clutch or brood except for the egg ejected by the parasite before laying. Life history and parasitism dynamics of the Shining Bronzecuckoo and its Gerygone hosts have been extensively studied in Australia (Brooker et al 1988;Brooker and Brooker 1989;Noske 2001) and New Zealand (Gill 1982a(Gill , b, 1983aAnderson et al 2013;Briskie 2003Briskie , 2007.…”

“…The Fan-tailed Gerygone from New Caledonia has two different nestling colour phenotypes, dark grey (dark hereafter) and pinkish-grey (bright hereafter), which can occur in monomorphic and polymorphic broods (Sato et al 2015;Attisano et al 2018). Although variation within the same brood could potentially lead to recognition errors (Stokke et al 2002;Moskát et al 2008), Fan-tailed Gerygone parents recognise and eject the parasite nestling within 24 h from hatching (Sato et al 2015;Attisano et al 2018). Grey Warblers from New Zealand also have polymorphic nestlings (Gill 1983b), but this species is neither an egg (Thorogood et al 2017) nor nestling ejector (J. Briskie, personal communication).…”