Alarm call‐based discrimination between common cuckoo and Eurasian sparrowhawk in a Chinese population of great tits

Morphological resemblance of the common cuckoo Cuculus canorus to the Eurasian sparrowhawk Accipiter nisus has been regarded as an example of predator mimicry. Common hosts could distinguish parasites as the result of coevolution, while rare hosts or non‐hosts may mistake cuckoos for hawks because rare hosts or non‐hosts behave similarly when faced with these two species. Birds usually produce alarm calls in addition to showing behavioral responses when in danger. However, previous studies of identification by rare hosts or non‐hosts of sparrowhawks usually lacked experimental evidence of alarm calls. Great tits Parus major, a rare cuckoo host, perform similar behaviors and usually produce alarm calls in response to sparrowhawks and common cuckoos. Here, we tested whether great tits could distinguish common cuckoo from sparrowhawk based on analysis of their alarm calls and the effects of playback of alarm calls on conspecific behavior. Previous studies showed that great tits have a complex communication system that conveys information about predators, and they could perform different kinds of response behavior to different alarm calls. If great tits have not made the ability to distinguish between common cuckoo and sparrowhawk, then their acoustic responses to these two species and their response behaviors in playback experiments should be similar. Specimens of a common cuckoo (parasite), a sparrowhawk (predator) and an Oriental turtle dove Streptopelia orientalis (harmless control) were used to elicit and subsequently record the response behavior and alarm calls of great tits. There was no significant difference in behavioral response among great tits when exposed to the dummy of cuckoo, sparrowhawk and dove. In contrast, they differed significantly in alarm calls. Great tits produced more notes per call that contained increasing D‐type and decreasing I‐type notes when responding to sparrowhawk as compared to cuckoo or dove. In playback experiments, we found that great tits responded more strongly to great tit hawk than to great tit cuckoo or great tit dove alarm calls. Our study suggests that great tits are able to distinguish sparrowhawks from common cuckoos and convey relevant information in alarm calls by adjusting the number and combinations of notes of a single call type.     

Host sexual selection and cuckoo parasitism: an analysis of nest size in sympatric and allopatric magpie Pica pica populations parasitized by the great spotted cuckoo Clamator glandarius

Magpies (Pica pica) build large nests that are the target of sexual selection, since males of early breeding pairs provide many sticks for nests and females mated to such males enjoy a material fitness benefit in terms of better quality territory and parental care of superior quality. Great spotted cuckoos (Clamator glandarius) preferentially parasitize large magpie nests and sexual selection for large nests is thus opposed by natural selection due to brood parasitism. Consistent with the hypothesized opposing selection pressures, in a comparative analysis of 14 magpie populations in Europe we found that nest volume was consistently smaller in sympatry than in allopatry with the great spotted cuckoo, in particular in areas with a high parasitism rate and high rates of rejection of mimetic model cuckoo eggs. These observations are consistent with the suggestion that magpies have evolved a smaller nest size in areas where cuckoos have exerted strong selection pressures on them in the recent past.     

Modeling the cuckoo’s brood parasitic behavior in the presence of egg polymorphism

The common cuckoo Cuculus canorus is a brood parasite that utilizes many host species. These have evolved defense against parasitism to reject cuckoo eggs that look unlike their own and some cuckoos have evolved egg mimicry to counter this defense. Egg phenotype indeed plays a key role for both the cuckoo and its hosts to successfully reproduce. It has been argued that cuckoos should parasitize host nests where egg phenotype matches because this makes parasitism more successful. Details of the cuckoo’s parasitic behavior, however, largely remains unknown if they really parasitize hosts depending on “egg matching”. In this paper, we model a time sequence of parasitic events in which a cuckoo finds host nests and decides to parasitize them or not in the presence of egg polymorphism. We evaluate which strategy is optimal: (1) opportunistic parasitism where cuckoos parasitize hosts irrespective of the phenotype, or (2) non-opportunistic parasitism where cuckoos parasitize hosts where egg phenotype matches. The analysis showed that either of the two strategies can be optimal. Factors not considered in the model, e.g., ecological and evolutionary changes both in the cuckoo and the host side, are discussed to explain apparent contrasts observed in some cuckoo–host interactions.     

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.     

Cuckoo–hawk mimicry? An experimental test

The similarity between many Old World parasitic cuckoos (Cuculinae) and Accipiter hawks, in size, shape and plumage, has been noted since ancient times. In particular, hawk-like underpart barring is more prevalent in parasitic than in non-parasitic cuckoos. Cuckoo-hawk resemblance may reflect convergent evolution of cryptic plumage that reduces detection by hosts and prey, or evolved mimicry of hawks by parasitic cuckoos, either for protection against hawk attacks or to facilitate brood parasitism by influencing host behaviour. Here, we provide the first evidence that some small birds respond to common cuckoos Cuculus canorus as if they were sparrowhawks Accipiter nisus. Great tits and blue tits were equally alarmed and reduced attendance at feeders during and after the presentation of mounted specimens of common cuckoos and sparrowhawks, but not in response to control presentations of collared doves or teal. Plumage manipulations revealed that the strong alarm response to cuckoos depended on their resemblance to hawks; cuckoos with barred underparts were treated like hawks, while those with unbarred underparts were treated like doves. However, barring was not the only feature inducing alarm because tits showed similarly strong alarm to barred and unbarred hawks, and little alarm to barred doves. These responses of tits, unsuitable as hosts and hence with no history of cuckoo parasitism, suggest that naive small birds can mistake cuckoos for hawks. Thus, any cuckoo-hawk discrimination by host species is likely to be an evolved response to brood parasitism.     

Change in host rejection behavior mediated by the predatory behavior of its brood parasite

Passerine hosts of parasitic cuckoos usually vary in their abilityto discriminate and reject cuckoo eggs. Costs of discriminationand rejection errors have been invoked to explain the maintenanceof this within-population variability. Recently, enforcementof acceptance by parasites has been identified as a rejectioncost in the magpie (Pica pica) and its brood parasite, the greatspotted cuckoo (Clamator glandarius). Previous experimentalwork has shown that rejecter magpies suffer from increased nestpredation by the great spotted cuckoo. Cuckoo predatory behavioris supposed to confer a selective advantage to the parasitebecause magpies experiencing a reproductive failure may providea second opportunity for the cuckoo to parasitize a replacementclutch. This hypothesis implicitly assumes that magpies modulatetheir propensity to reject parasite eggs as a function of previousexperience. We tested this hypothesis in a magpie populationbreeding in study plots varying in parasitism rate. Magpie pairs thatwere experimentally parasitized and had their nests depredated,after their rejection behavior had been assessed, changed theirbehavior from rejection to acceptance. The change in host behaviorwas prominent in study plots with high levels of parasitism,but not in plots with rare or no cuckoo parasitism. We discussthree possible explanations for these differences, concludingthat in study plots with a high density of cuckoos, the probability fora rejecter magpie nest of being revisited and depredated bya cuckoo is high, particularly for replacement clutches, and,therefore, the cost for magpies of rejecting a cuckoo egg ina replacement clutch is increased. Moreover, in areas with highlevels of host defense (low parasitism rate), the probabilityof parasitism and predation of rejecter-magpie nests by thecuckoo is reduced in both first and replacement clutches. Therefore,rejecter magpies in such areas should not change their rejectionbehavior in replacement clutches.     

Cuckoo parasitism in a cavity nesting host: near absent egg‐rejection in a northern redstart population under heavy apparent (but low effective) brood parasitism

Brood parasite – host systems continue to offer insights into species coevolution. A notable system is the redstart Phoenicurus phoenicurus parasitized by the ‘redstart‐cuckoo’ Cuculus canorus gens. Redstarts are the only regular cuckoo hosts that breed in cavities, which challenges adult cuckoos in egg laying and cuckoo chicks in host eviction. We investigated parasitism in this system and found high overall parasitism rates (31.1% of 360 redstart nests), but also that only 33.1% of parasitism events (49 of 148 eggs) were successful in laying eggs into redstart nest cups. The majority of cuckoo eggs were mislaid and found on the rim of the nest; outside the nest cup. All available evidence suggests these eggs were not ejected by hosts. The effective parasitism rate was therefore only 12.8% of redstart nests. Redstarts responded to natural parasitism by deserting their nests in 13.0% of cases, compared to desertion rates of 2.8% for non‐parasitized nests. Our egg parasitism experiments found low rates (12.2%) of rejection of artificial non‐mimetic cuckoo eggs. Artificial mimetic and real cuckoo eggs added to nests were rejected at even lower rates, and were always rejected via desertion. Under natural conditions, only 21 cuckoo chicks fledged of 150 cuckoo eggs laid. Adding to this low success, is that cuckoo chicks are sometimes unable to evict all host young, and were more likely to die as a result compared to cuckoo chicks reared alone. This low success seems to be mainly due to the cavity nesting strategy of the redstart which is a challenging obstacle for the cuckoo. The redstart‐cuckoo system appears to be a fruitful model system and we suggest much more emphasis should be placed on frontline defences such as nest site selection strategies when investigating brood parasite–host coevolution.     

Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population

Parasitic cuckoos lay eggs that mimic those of their hosts, and such close phenotypic matching may arise from coevolutionary interactions between parasite and host. However, cuckoos may also explicitly choose hosts in a way that increases degree of matching between eggs of cuckoos and parasites, with female preference for specific host phenotypes increasing the degree of matching. We tested for temporal change in degree of matching between eggs of the parasitic European cuckoo (Cuculus canorus) and its reed warbler (Acrocephalus scirpaceus) host during 24 consecutive years in a recently parasitized reed warbler population. Cuckoo-host egg matching in an ultraviolet-brownness component yielding most of the chromatic variance of eggs improved during the study period. Improved matching was not due to changes in cuckoo egg phenotype. Cuckoo eggs matched host eggs for ultraviolet-brownness within nests irrespective of duration of sympatry. Ultraviolet-brownness of cuckoo eggs was similar to that of reed warbler eggs at parasitized nests, but differed from that of reed warbler eggs at unparasitized nests. These findings provide tentative support for the cuckoo preference hypothesis suggesting that cuckoo-host egg matching could partially be due to cuckoo females selecting host nests based on the appearance of their eggs.     

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.     

Egg shape mimicry in parasitic cuckoos

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo–host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan‐tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo–host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo–host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo–host systems.     

Brood parasitism is associated with increased bacterial contamination of host eggs: bacterial loads of host and parasitic eggs

Factors related to bacterial environment of nests are of primary interest for understanding the causes of embryo infection and the evolution of antimicrobial defensive traits in birds. Nest visitors such as parasites could act as vectors for bacteria and/or affect the hygienic conditions of nests and hence influence the nest bacterial environment. In the present study, we explored some predictions of this hypothetical scenario in the great spotted cuckoo (Clamator glandarius)–magpie (Pica pica) system of brood parasitism. Great spotted cuckoos visit the nests of their magpie hosts and frequently damage some of the host eggs when laying eggs or on subsequent visits. Therefore, it represents a good system for testing the effect of nest visitors on the bacterial environment of nests. In accordance with this hypothesis, we found that the bacterial load of magpie eggshells was greater in parasitized nests, which may suggest that brood parasitism increases the probability of bacterial infection of magpie eggs. Moreover, comparisons of bacterial loads of cuckoo and magpie eggs revealed that: (1) cuckoo eggshells harboured lower bacterial densities than those of their magpie hosts in the same nests and (2) the prevalence of bacteria inside unhatched eggs was higher for magpies than for great spotted cuckoos. These interspecific differences were predicted because brood parasitic eggs (but not host eggs) always experience the bacterial environments of parasitized nests. Therefore, the results obtained in the present study suggest that parasitic eggs are better adapted to environments with a high risk of bacterial contamination than those of their magpie hosts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 836–848.     

Brood-parasite interactions between great spotted cuckoos and magpies: a model system for studying coevolutionary relationships

Brood parasitism is one of the systems where coevolutionary processes have received the most research. Here, we review experiments that suggest a coevolutionary process between the great spotted cuckoo (Clamator glandarius) and its magpie (Pica pica) host. We focus on different stages of establishment of the relationship, from cuckoos selecting individual hosts and hosts defending their nests from adult cuckoos, to the ability of magpies to detect cuckoo eggs in their nests. Novel coevolutionary insights emerge from our synthesis of the literature, including how the evolution of "Mafia" behaviour in cuckoos does not necessarily inhibit the evolution of host recognition and rejection of cuckoo offspring, and how different populations of black-billed magpies in Europe have evolved specific host traits (e.g. nest and clutch size) as a result of interactions with the great spotted cuckoo. Finally, the results of the synthesis reveal the importance of using a meta-population approach when studying coevolution. This is especially relevant in those cases where gene flow among populations with different degrees of brood parasitism explains patterns of coexistence between defensive and non-defensive host phenotypes. We propose the use of a meta-population approach to distinguish between the "evolutionary equilibrium" hypothesis and the "evolutionary lag" hypothesis.     

Birds respond similarly to taxidermic models and live cuckoos <Emphasis Type="Italic">Cuculus canorus</Emphasis>

Stuffed birds are widely used in research for identifying effects of predators and nest parasites on bird behaviour, studying levels of aggression and the size of territories. However, the fact that these models do not move or vocalize may question the results of such studies and open them to criticism. One solution would be to determine how the results of research using stuffed dummies correlate with the response of wild animals to enemies under the same environmental conditions. In a first attempt, we examined the correlation between the intensity of mobbing of a dummy cuckoo Cuculus canorus and interactions with live cuckoos in the field during the breeding season in western Poland. A total of 39 bird species mobbed cuckoo dummies; all 39 were found to attack live cuckoos, while 24 species (61.5%) did so during experiments using a dummy. The number of individual birds involved in mobbing a dummy was positively correlated with the number of individuals attacking real cuckoos in the same areas, even when the most commonly mobbing species, the barn swallow Hirundo rustica, was excluded from the analyses. However, we did not find significant differences in frequency of mobbing behaviour depending on cuckoo behaviour described as flight or sitting, or calling rather than remaining quiet. Therefore, we conclude that the use of a dummy for studying mobbing of hosts and non-hosts of the cuckoo provide results that are similar to those made in response to the behaviour of live hosts.     

Complex feeding behaviour by magpies in nests with great spotted cuckoo nestlings

Parent decisions about food allocation are usually based on simple time‐saving rules that optimize their own fitness; however, they can sometimes vary depending on the prevailing ecological conditions both outside and inside the nest. Parent–offspring interactions also become more complex when parents suffer from brood parasitism, which implies that they care for the parasite's eggs and unrelated young. The great spotted cuckoo Clamator glandarius is a specialist brood parasite that uses the magpie Pica pica as its primary host. Here, by filming food allocation by magpie parents in natural non‐parasitized and experimentally parasitized and non‐parasitized magpie nests, we have found that magpie provisioning behaviour is highly complex including two types of feedings apart from normal ones. First, false feedings, when the parent touched the chick's beak but did not leave any food, occurred more frequently when feeding a cuckoo than when feeding magpie nestlings. Second, two types of what we have called coax feedings: 2a) when magpie parents induce a nestling to beg by waking it up by touching it softly with the beak, and 2b) when parents disregard begging signals (always from brood parasitic great spotted cuckoos) while coaxing one non‐begging nestling (always one of their own) to feed it. We suggest that brood parasitism, involving selfish excessively begging nestlings, could have acted as a selective pressure for both false and coax feedings to evolve, as both imply ignoring nestlings that beg too much. We also discuss that these parental responses could have evolved either by a discrimination without recognition mechanism, or, more probably, by a recognition‐based discrimination mechanism.     

Continuous Variation Rather than Specialization in the Egg Phenotypes of Cuckoos (Cuculus canorus) Parasitizing Two Sympatric Reed Warbler Species

The evolution of brood parasitism has long attracted considerable attention among behavioural ecologists, especially in the common cuckoo system. Common cuckoos (Cuculus canorus) are obligatory brood parasites, laying eggs in nests of passerines and specializing on specific host species. Specialized races of cuckoos are genetically distinct. Often in a given area, cuckoos encounter multiple hosts showing substantial variation in egg morphology. Exploiting different hosts should lead to egg-phenotype specialization in cuckoos to match egg phenotypes of the hosts. Here we test this assumption using a wild population of two sympatrically occurring host species: the great reed warbler (Acrocephalus arundinaceus) and reed warbler (A. scirpaceus). Using colour spectrophotometry, egg shell dynamometry and egg size measurements, we studied egg morphologies of cuckoos parasitizing these two hosts. In spite of observing clear differences between host egg phenotypes, we found no clear differences in cuckoo egg morphologies. Interestingly, although chromatically cuckoo eggs were more similar to reed warbler eggs, after taking into account achromatic differences, cuckoo eggs seemed to be equally similar to both host species. We hypothesize that such pattern may represent an initial stage of an averaging strategy of cuckoos, that – instead of specializing for specific hosts or exploiting only one host – adapt to multiple hosts.     

Diet specialization and brood parasitism in cuckoo species

1. Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.
2. In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.
3. After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.
4. The findings of this study provide an additional understanding of the cuckoos’ ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

     

Brood parasites lay eggs matching the appearance of host clutches

Interspecific brood parasitism represents a prime example of the coevolutionary arms race where each party has evolved strategies in response to the other. Here, we investigated whether common cuckoos (Cuculus canorus) actively select nests within a host population to match the egg appearance of a particular host clutch. To achieve this goal, we quantified the degree of egg matching using the avian vision modelling approach. Randomization tests revealed that cuckoo eggs in naturally parasitized nests showed lower chromatic contrast to host eggs than those assigned randomly to other nests with egg-laying date similar to naturally parasitized clutches. Moreover, egg matching in terms of chromaticity was better in naturally parasitized nests than it would be in the nests of the nearest active non-parasitized neighbour. However, there was no indication of matching in achromatic spectral characteristics whatsoever. Thus, our results clearly indicate that cuckoos select certain host nests to increase matching of their own eggs with host clutches, but only in chromatic characteristics. Our results suggest that the ability of cuckoos to actively choose host nests based on the eggshell appearance imposes a strong selection pressure on host egg recognition.     

Eavesdropping cuckoos: further insights on great spotted cuckoo preference by magpie nests and egg colour

Reproductive success of brood parasites largely depends on appropriate host selection and, although the use of inadvertent social information emitted by hosts may be of selective advantage for cuckoos, this possibility has rarely been experimentally tested. Here, we manipulated nest size and clutch colouration of magpies (Pica pica), the main host of great spotted cuckoos (Clamator glandarius). These phenotypic traits may potentially reveal information about magpie territory and/or parental quality and could hence influence the cuckoo’s choice of host nests. Experimentally reduced magpie nests suffered higher predation rate, and prevalence of cuckoo parasitism was higher in magpie nests with the densest roofs, which suggests a direct advantage for great spotted cuckoos choosing this type of magpie nest. Colouration of magpie clutches was manipulated by adding one artificial egg (blue or cream colouration) at the beginning of the egg-laying period. We found that host nests holding an experimental cream egg experienced a higher prevalence of cuckoo parasitism than those holding a blue-coloured egg. Results from these two experiments suggest that great spotted cuckoos cue on magpie nest characteristics and the appearance of eggs to decide parasitism, and confirm, for the first time, the ability of cuckoos to distinguish between eggs of different colours within the nest of their hosts. Several hypothetical scenarios explaining these results are discussed.     

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.     

Isolation by time and habitat and coexistence of distinct host races of the common cuckoo

Isolation by time occurs when different populations of a single species reproduce at different times and thereby reduce the probability of interbreeding, potentially causing divergent adaptation to timing of reproduction, eventually resulting in ecological species separated by timing of reproduction. We analysed extensive data on timing of reproduction by different host races of the common cuckoo Cuculus canorus that is an obligate brood parasite laying eggs in the nests of many different species of passerine birds. Because different hosts breed at different times, specific host races of cuckoos have adapted to specific hosts by laying eggs when nests of these hosts are available, and such divergence may be further exaggerated by differences in timing of breeding among host races with similar habitat requirements. Host species accounted for a quarter of the variance in timing of breeding by the cuckoo. Common cuckoos reproduced at a similar, but narrower subset of dates as did possible hosts, showing that only a fraction of hosts with specific breeding dates were parasitized. Common cuckoo eggs laid in the 'right' kind of nests, phenotypically matching the eggs of the host, were laid later during the season than cuckoo eggs laid in the 'wrong' kind of nests where the eggs did not mimic those of the host. Pairs of sympatric cuckoo host races differed more in timing of breeding than pairs of allopatric host races, and pairs of cuckoo host races with similar breeding habitat differed more in breeding date than pairs of cuckoo host races with dissimilar habitat, as expected from reproductive character displacement. These findings are consistent with cuckoo host races being isolated by timing of breeding and habitat.