The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Egg mimicry by the Pacific koel: mimicry of one host facilitates exploitation of other hosts with similar egg types

When brood parasites exploit multiple host species, egg rejection by hosts may select for the evolution of host‐specific races, where each race mimics a particular host's egg type. However, some brood parasites that exploit multiple hosts with the ability to reject foreign eggs appear to have only a single egg type. In these cases, it is unclear how the parasite egg escapes detection by its hosts. Three possible explanations are: 1) host‐specific races are present, but differences in egg morphology are difficult for the human eye to detect; 2) the brood parasite evolves a single egg type that is intermediate in appearance between the eggs of its hosts; 3) or the parasite evolves mimicry of one of its hosts, which subsequently allows it to exploit other species with similar egg morphology. Here we test these possibilities by quantifying parameters of egg appearance of the brood‐parasitic Pacific koel Eudynamys orientalis and seven of its hosts. Koel eggs laid in the nests of different hosts did not show significant differences in colour or pattern, suggesting that koels have not evolved host‐specific races. Koel eggs were similar in colour, luminance and pattern to the majority of hosts, but were significantly more similar in colour and luminance to one of the major hosts than to two other major hosts, supporting hypothesis 3. Our findings suggest that mimicry of one host can allow a brood parasite to exploit new hosts with similar egg morphologies, which could inhibit the evolution of host defences in naïve hosts.     

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.     

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasite's reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.     

Experimental Shifts in Intraclutch Egg Color Variation Do Not Affect Egg Rejection in a Host of a Non-Egg-Mimetic Avian Brood Parasite

Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host’s ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins’ behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.     

To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti‐parasite strategies

Hosts either tolerate avian brood parasitism or reject it by ejecting parasitic eggs, as seen in most rejecter hosts of common cuckoos, Cuculus canorus, or by abandoning parasitized clutches, as seen in most rejecter hosts of brown‐headed cowbirds, Molothrus ater. What explains consistent variation between alternative rejection behaviours of hosts within the same species and across species when exposed to different types of parasites? Life history theory predicts that when parasites decrease the fitness of host offspring, but not the future reproductive success of host adults, optimal clutch size should decrease. Consistent with this prediction, evolutionarily old cowbird hosts, but not cuckoo hosts, have lower clutch sizes than related rarely‐ or newly parasitized species. We constructed a mathematical model to calculate the fitness payoffs of egg ejector vs. nest abandoner hosts to determine if various aspects of host life history traits and brood parasites’ virulence on adult and young host fitness differentially influence the payoffs of alternative host defences. These calculations showed that in general egg ejection was a superior anti‐parasite strategy to nest abandonment. Yet, increasing parasitism rates and increasing fitness values of hosts’ eggs in both currently parasitized and future replacement nests led to switch points in fitness payoffs in favour of nest abandonment. Nonetheless, nest abandonment became selectively more favourable only at lower clutch sizes and only when hosts faced parasitism by a cowbird‐ rather than a cuckoo‐type brood parasite. We suggest that, in addition to evolutionary lag and gape‐size limitation, our estimated fitness differences based on life history trait variation provide new insights for the consistent differences observed in the anti‐parasite rejection strategies between many cuckoo‐ and cowbird‐hosts.     

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.     

Long‐term coevolution between avian brood parasites and their hosts

Coevolutionary theory predicts that the most common long‐term outcome of the relationships between brood parasites and their hosts should be coevolutionary cycles based on a dynamic change selecting the currently least‐defended host species, given that when well‐defended hosts are abandoned, hosts will be selected to decrease their defences as these are usually assumed to be costly. This is assumed to be the case also in brood parasite‐host systems. Here I examine the frequency of the three potential long‐term outcomes of brood parasite–host coevolution (coevolutionary cycles, lack of rejection, and successful resistance) in 182 host species. The results of simple exploratory comparisons show that coevolutionary cycles are very scarce while the lack of rejection and successful resistance, which are considered evolutionary enigmas, are much more frequent. I discuss these results considering (i) the importance of different host defences at all stages of the breeding cycle, (ii) the role of phenotypic plasticity in long‐term coevolution, and (iii) the evolutionary history of host selection. I suggest that in purely antagonistic coevolutionary interactions, such as those involving brood parasites and their hosts, that although cycles will exist during an intermediate phase of the interactions, the arms race will end with the extinction of the host or with the host acquiring successful resistance. As evolutionary time passes, this resistance will force brood parasites to use previously less suitable host species. Furthermore, I present a model that represents the long‐term trajectories and outcomes of coevolutionary interactions between brood parasites and their hosts with respect to the evolution of egg‐rejection defence. This model suggests that as an increasing number of species acquire successful resistance, other unparasitized host species become more profitable and their parasitism rate and the costs imposed by brood parasitism at the population level will increase, selecting for the evolution of host defences. This means that although acceptance is adaptive when the parasitism rate and the costs of parasitism are very low, this cannot be considered to represent an evolutionary equilibrium, as conventional theory has done to date, because it is not stable.     

A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite

Avian brood parasites reduce the reproductive output of their hosts and thereby select for defence mechanisms such as ejection of parasitic eggs. Such defence mechanisms simultaneously select for counter-defences in brood parasites, causing a coevolutionary arms race. Although coevolutionary models assume that defences and counter-defences are genetically influenced, this has never been demonstrated for brood parasites. Here, we give strong evidence for genetic differences between ejector and nonejectors, which could allow the study of such host defence at the genetic level, as well as studies of maintenance of genetic variation in defences. Briefly, we found that magpies, that are the main host of the great spotted cuckoo in Europe, have alleles of one microsatellite locus (Ase64) that segregate between accepters and rejecters of experimental parasitic eggs. Furthermore, differences in ejection rate among host populations exploited by the brood parasite covaried significantly with the genetic distance for this locus.     

Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo

Brood parasites dramatically reduce the reproductive successof their hosts, which therefore have developed defenses againstbrood parasites. The first line of defense is protecting thenest against adult parasites. When the parasite has successfullyparasitized a host nest, some hosts are able to recognize andreject the eggs of the brood parasite, which constitutes the secondline of defense. Both defense tactics are costly and would be counteractedby brood parasites. While a failure in nest defense implies successfulparasitism and therefore great reduction of reproductive successof hosts, a host that recognizes parasitic eggs has the opportunityto reduce the effect of parasitism by removing the parasiticegg. We hypothesized that, when nest defense is counteractedby the brood parasite, hosts that recognize cuckoo eggs shoulddefend their nests at a lower level than nonrecognizers becausethe former also recognize adult cuckoos. Magpie (Pica pica) hoststhat rejected model eggs of the brood parasitic great spottedcuckoo (Clamator glandarius) showed lower levels of nest defensewhen exposed to a great spotted cuckoo than when exposed toa nest predator (a carrion crow Corvus corone). Moreover, magpiesrejecting cuckoo eggs showed lower levels of nest defense againstgreat spotted cuckoos than nonrecognizer magpies, whereas differencesin levels of defense disappeared when exposed to a carrion crow.These results suggest that hosts specialize in antiparasitedefense and that different kinds of defense are antagonistically expressed.We suggest that nest-defense mechanisms are ancestral, whereasegg recognition and rejection is a subsequent stage in the coevolutionaryprocess. However, host recognition ability will not be expressedwhen brood parasites break this second line of defense.     

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.     

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences

Arms races between avian brood parasites and their hosts often result in parasitic mimicry of host eggs, to evade rejection. Once egg mimicry has evolved, host defences could escalate in two ways: (i) hosts could improve their level of egg discrimination; and (ii) negative frequency-dependent selection could generate increased variation in egg appearance (polymorphism) among individuals. Proficiency in one defence might reduce selection on the other, while a combination of the two should enable successful rejection of parasitic eggs. We compared three highly variable host species of the Afrotropical cuckoo finch Anomalospiza imberbis, using egg rejection experiments and modelling of avian colour and pattern vision. We show that each differed in their level of polymorphism, in the visual cues they used to reject foreign eggs, and in their degree of discrimination. The most polymorphic host had the crudest discrimination, whereas the least polymorphic was most discriminating. The third species, not currently parasitized, was intermediate for both defences. A model simulating parasitic laying and host rejection behaviour based on the field experiments showed that the two host strategies result in approximately the same fitness advantage to hosts. Thus, neither strategy is superior, but rather they reflect alternative potential evolutionary trajectories.     

AVIAN BROOD PARASITISM: INFORMATION USE AND VARIATION IN EGG‐REJECTION BEHAVIOR

Hosts of avian brood parasites often vary in their response to parasitized clutches: they may eject one or several eggs, desert the nest, or accept all the eggs. Focusing on hosts exposed to single‐egg parasitism by an evicting brood parasite, we construct an optimality model that includes all these behavioral options and use it to explore variation in rejection behavior. We particularly consider the influence of egg mimicry and external cues (observations of adult parasites near the nest) on optimal choice of rejection behavior. We find that several rejection responses will be present in a host population under a wide range of conditions. Ejection of multiple eggs tends to be adaptive when egg mimicry is fairly accurate, external cues provide reliable information of the risk of parasitism, and the expected success of renesting is low. If the perceived risk of parasitism is high, ejection of one or a few eggs may be the optimal rejection response even in cases in which hosts cannot discriminate between eggs. This may have consequences for the long‐term outcome of the coevolutionary chase between hosts and parasites. We propose an alternative evolutionary pathway by which egg ejection may first arise as a defense against brood parasitism.     

Absence of egg discrimination in a suitable cuckoo Cuculus canorus host breeding away from trees

There is at present considerable variation in the level of antiparasite defences among different host species of avian brood parasites, but in many potential hosts some individuals reject poorly matching parasite eggs. Here we present unique absence of egg discrimination behaviour backed up by a lack of egg recognition abilities in a suitable common cuckoo Cuculus canorus host, the skylark Alauda arvensis. Skylarks did not show any clear rejection response to experimentally added highly non‐mimetic foreign eggs in any behavioural context, even before they had started laying or when the whole clutch was exchanged with foreign eggs. This absence of antiparasite defence can be explained by the breeding habitat of larks consisting of largely treeless open landscapes where cuckoos have little access to the nests, thereby eroding the possibility of coevolutionary interactions. Our results are strikingly consistent with the spatial habitat structure hypothesis proposed to explain the occurrence and extent of avian host‐parasite co‐adaptation.     

Relic behaviours, coevolution and the retention versus loss of host defences after episodes of avian brood parasitism

Most previous studies of brood parasitism have stressed that host defences, such as egg recognition, are lost in the absence of parasitism. Such losses could result in coevolutionary cycles in which parasites shift away from well-defended hosts only to switch back to them later at a time when these hosts have lost much or all of their defences and the parasite's current hosts have built up effective defences. However, the alternative 'single trajectory' model predicts that parasites rarely switch back to old hosts because ex-hosts retain egg recognition for long periods in the absence of parasitism. If true, egg recognition by the host may be a 'relic behaviour', because in the absence of parasitism its adaptive value is close to neutral. Using artificial nonmimetic eggs, I tested for egg recognition in two populations that are currently unparasitized but that are descended from lineages likely to have been parasitized in the past: the grey catbird, Dumetella carolinensis, on Bermuda and the loggerhead shrike, Lanius ludovicianus, in California. Both of these populations showed long-term retention, ejecting nonmimetic eggs at rates of nearly 100%. Because potential present-day selection pressures, such as conspecific parasitism, do not explain this egg recognition, Bermuda catbirds apparently retain recognition from North American conspecifics that were cowbird hosts before colonizing Bermuda and shrikes retain recognition from Old World congeners that were hosts of cuckoos. Retention is also indicated by passerines in California and the Caribbean that had high rejection rates of nonmimetic eggs before coming into contact with cowbirds. These new data suggest that both the coevolutionary cycles and single trajectory models have importance and that rejection behaviour can have insignificant costs, which is consistent with evolutionary lag explanations for the acceptance of parasitic eggs shown by some cuckoo and many cowbird hosts. Copyright 2001 The Association for the Study of Animal Behaviour.     

Host selection in parasitic birds: are open‐cup nesting insectivorous passerines always suitable cuckoo hosts?

How do potential hosts escape detrimental interactions with brood parasites? Current consensus is that hole‐nesting and granivorous birds avoid brood parasites, like common cuckoos Cuculus canorus, by their inaccessible nest‐sites and food unsuitable for parasites, respectively. Any open‐nesting insectivorous hosts are believed to remain open to brood parasite exploitation which leads to the evolution of costly host defences like egg or chick discrimination. In contrast to this coevolutionary scenario, we show for the first time that a previously not studied but seemingly suitable host species escapes brood parasites. The Asian verditer flycatcher Eumyias thalassinus, feed newly hatched chicks entirely with beetles and grasshoppers. These are poor quality and hard to digest diet items that are rarely fed to own or cuckoo chicks by regular hosts. Indeed, chick cross‐fostering experiments showed that these food items remained undigested by either cuckoos or other sympatric passerines causing them to die quickly. Egg discrimination experiments showed that the flycatcher accepts any foreign eggs. Although most but not all other potential explanations can be safely excluded at present, the most parsimonious historical explanation for these patterns is that the flycatcher exploits a trophic niche that no other sympatric bird can exploit, and that any cuckoo lineages that switch from their original hosts to the flycatcher have no possibilities for establishing viable populations. Thus, the current classification of host suitability based on diet composition may need revision, raising an important cautionary tale for comparative studies and the interpretation of apparent host rejection of parasitic chicks.     

When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model

It has been suggested that discrimination and rejection of thenestlings of avian brood parasites are most likely to evolvewhen the parasite nestling is raised alongside the host nestlings,for example, many cowbird-host systems. Under these circumstances,the benefits of discrimination are high because the host parentsmay save most of their brood. However, there is a general absenceof nestling rejection behavior among hosts of nonevicting parasites.In a cost-benefit equilibrium model, based on the premise thathost species learn to recognize their offspring through imprintingon first breeding, we show that nestling recognition can beadaptive for hosts of cowbirds, but only under strict conditions.Namely, when host nestling survival alongside the parasite islow, rates of parasitism are high and the average clutch sizeis large. All of these conditions are seldom simultaneouslyachieved in real systems. Most importantly, the parasite nestling,on average, does not sufficiently depress host nestling survivalto outweigh the costs of nestling recognition and rejectionerrors. Thus, we argue that nestling acceptance behaviors byhosts of nonevicting brood parasites may be explained as anevolutionary equilibrium in which recognition costs act as astabilizing selection pressure against rejection when most ofthe host's offspring survive parasitism.     

Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not?

Mimicry is one of the most conspicuous and puzzling phenomena in nature. The best-known examples come from insects and brood parasitic birds. Unfortunately, the term 'mimicry' is used indiscriminately and inconsistently in the brood parasitic literature despite the obvious fact that similarities of eggs, nestlings and adults of brood parasites to their hosts could result from many different processes (phylogenetic constraint, predation, intraspecific arms-races, vocal imitation, exploitation of pre-existing preferences, etc.). In this note I wish to plead for a more careful use of the term. I review various processes leading to a similarity between propagules (both eggs and nestlings) of brood parasites and their hosts and stress that: (1) mimetic and non-mimetic similarities should be differentiated, (2) a mere similarity of host and parasite propagules provides no evidence for mimicry, (3) mimicry is more usefully understood as a (coevolutionary) process rather than an appearance, and (4) mimicry terminology should reflect the process which led to mimetic similarity. Accepting the mimicry hypothesis requires both the experimental approach and rejection of alternative hypotheses explaining similarities of host and parasite propagules.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 69–78.     

MAGPIE HOST MANIPULATION BY GREAT SPOTTED CUCKOOS: EVIDENCE FOR AN AVIAN MAFIA?

Why should the hosts of brood parasites accept and raise parasitic offspring that differ dramatically in appearance from their own? There are two solutions to this evolutionary enigma. (1) Hosts may not yet have evolved the capability to discriminate against the parasite, or (2) parasite-host systems have reached an evolutionary equilibrium. Avian brood parasites may either gain renesting opportunities or force their hosts to raise parasitic offspring by destroying or preying upon host eggs or nestlings following host ejection of parasite offspring. These hypotheses may explain why hosts do not remove parasite offspring because only then will hosts avoid clutch destruction by the cuckoo. Here we show experimentally that if the egg of the parasitic great spotted cuckoo Clamator glandarius is removed from nests of its magpie Pica pica host, nests suffer significantly higher predation rates than control nests in which parasite eggs have not been removed. Using plasticine model eggs resembling those of magpies and observations of parasites, we also confirm that great spotted cuckoos that have laid an ejected egg are indeed responsible for destruction of magpie nests with experimentally ejected parasite eggs. Cuckoos benefit from destroying host offspring because they thereby induce some magpies to renest and subsequently accept a cuckoo egg.