Multiple costs are relevant for evolution of host anti-parasite defences. Reply to Yang C et al . (2018).

Abstract

Studies of brood parasite-host coevolution have generally assumed that hosts invest more parental care to rear parasite progeny than their own offspring: this view was taken for granted in cases when a parasite chick (e.g. the common cuckoo Cuculus canorus; hereafter 'cuckoo') was dramatically larger than a host chick (small passerines in the case of cuckoos [1]). This seemed obvious because a cuckoo fledgling weighs as much as the whole family of a host, i.e. all chicks and both male and female fosterers combined (own unpublished data). Recently, we reported results that question this view: rearing the cuckoo was not associated with overall higher immediate rearing costs to common redstarts Phoenicurus phoenicurus (hereafter 'redstart') above the natural baseline levels that are imposed by efforts to rear their own progeny anyway [2]. Additionally, we suggested that such low costs may partly help explain low levels of host counterdefences in this host. In their comment, Yang et al.[3] do not contradict our main conclusions (rearing the cuckoo is not extra costly) but disagree with our suggestion that surprisingly low immediate rearing costs can be relevant for the evolution of host defences. Here, we address this criticism.Yang et al.[3] claim that individual hosts that are successfully parasitized by cuckoos do not contribute their genes to the next generation, which provides a strong selective pressure on hosts, whereas an excessive parental care for parasite progeny can hardly drive the evolution of anti-parasitic adaptation in hosts. Further, [3] argue that even if the immediate costs of rearing a cuckoo chick do not exist, parasitism itself should be sufficient to promote anti-parasitic defences in hosts.We agree that the loss of the host's own progeny after successful parasitism is the most important cost that provides a strong selective pressure on hosts to evolve defences. We also agree that the loss of progeny per se is sufficient to promote anti-parasitic defences in hosts even in the potential absence of immediate rearing costs. However, all this does not mean that other costs are irrelevant. Indeed, the lost progeny cost is the same or very similar in all regular cuckoo hosts because the cuckoo chick kills all its nest-mates in all host species [1] (with a single exception of redstarts); therefore such invariable lost progeny cost cannot explain the large variability in host defences. Therefore, we suggest that multiple costs-i.e. not only the lost progeny cost-play a non-negligible role in the evolution of anti-parasitic defences and can thus better explain variability in levels of anti-parasitic defences across various host species.Such costs include high demands to raise the cuckoo because host parents exhausted by care for the cuckoo more likely fail to transmit their genes in potential next breeding attempts when caring for their own progeny (i.e. the trade-off between the current and future reproduction). Specifically, in the redstart, [2] reviewed factors considered by previous studies as impo...