Brood parasitism selects for no defence in a cuckoo host

Abstract

In coevolutionary arms races, like between cuckoos and their hosts, it is easy to understand why the host is under selection favouring anti-parasitism behaviour, such as egg rejection, which can lead to parasites evolving remarkable adaptations to 'trick' their host, such as mimetic eggs. But what about cases where the cuckoo egg is not mimetic and where the host does not act against it? Classically, such apparently non-adaptive behaviour is put down to evolutionary lag: given enough time, egg mimicry and parasite avoidance strategies will evolve. An alternative is that absence of egg mimicry and of anti-parasite behaviour is stable. Such stability is at first sight highly paradoxical. I show, using both field and experimental data to parametrize a simulation model, that the absence of defence behaviour by Cape bulbuls (Pycnonotus capensis) against parasitic eggs of the Jacobin cuckoo (Clamator jacobinus) is optimal behaviour. The cuckoo has evolved massive eggs (double the size of bulbul eggs) with thick shells, making it very hard or impossible for the host to eject the cuckoo egg. The host could still avoid brood parasitism by nest desertion. However, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg, a strategy aided by the fact that many cuckoo eggs are incorrectly timed, so do not hatch in time and hence do not reduce host fitness to zero. Selection will therefore prevent the continuation of any coevolutionary arms race. Non-mimetic eggs and absence of defence strategies against cuckoo eggs will be the stable, if at first sight paradoxical, result.

Why cuckoos should parasitize parrotbills by laying eggs randomly rather than laying eggs matching the egg appearance of parrotbill hosts?

“…For example, the mobbing by the bulbul (Pycnonotus capensis) makes it difficult for the female Jacobin cuckoo (Clamator jacobinus) to gain access to the host nest, but also difficult to monitor host behavior and hence time her laying correctly. In the end, many cuckoo eggs are laid too late and fail to hatch (Liversidge 1970;Krüger 2011). Furthermore, exposure, when laying eggs, also increases the rejection rate of cuckoo eggs because hosts may enhance their ability to discriminate against foreign eggs from increased risk of parasitism (e.g.…”

“…Detection, mobbing or attack by hosts are costly for cuckoos. Mobbing or attack by hosts may cause failure of egg-laying, injury and even have lethal consequence for adult cuckoos (Liversidge 1970;Davies 2000Davies , 2011Røskaft et al 2002;Krüger 2011). For example, the mobbing by the bulbul (Pycnonotus capensis) makes it difficult for the female Jacobin cuckoo (Clamator jacobinus) to gain access to the host nest, but also difficult to monitor host behavior and hence time her laying correctly.…”

Interspecific egg rejection as ecological collateral damage from selection driven by conspecific brood parasitism

“…In these species, it is unclear whether this reflects variation among individuals in cognitive aspects of recognition or variation in the recognition cues or social environment that an individual happens to encounter (Davies et al, 1996;Rothstein, 1982). Understanding why hosts vary in defenses against parasitism remains an important area of inquiry, and a number of factors have been identified to explain why such traits are lacking in some species or individuals within species (Davies, 1999;Kruger, 2011;Moskat and Hauber, 2007;Røskaft et al, 2006;Rothstein, 1990;Underwood and Sealy, 2006). Brood parasitism within species also occurs in birds, having been documented in over 200 species (Andersson, 1984;Lyon and Eadie, 2008;Yom-Tov, 1980.…”

Can nest predation explain the lack of defenses against cowbird brood parasitism in the Rufous-collared Sparrow (Zonotrichia capensis)?

“…As we showed in the simulations, there is no adaptive advantage of nest desertion following parasitism, because any new nesting attempt will have a high probability of being parasitized and/or will have a low probability of success. Therefore, an apparent evolutionary lag is generated because of the tradeoff between the costs and benefits of the antiparasite strategies (Krüger 2011). It is possible that additional costs associated with antiparasite strategies such as recognition errors and the accidental breakage of a bird's own eggs when trying to eject a parasite egg (Lotem et al 1992, Lotem andNakamura 1998), as well as passive benefits such as a dilution effect generated by the presence of parasite eggs in the nest (Gloag et al 2012), could make the evolution of antiparasite defenses unlikely.…”

“…This evidence led us to speculate that sparrows may have had sufficient time to evolve antiparasite defenses if such defenses were strongly favored by selection. An alternative hypothesis proposes that there are morphological or ecological constraints that would explain the lack of defenses in some hosts (Krüger 2011). These constraints result in an evolutionary equilibrium whereby the costs of the evolution of antiparasite defenses exceed the benefits.…”