AVIAN BROOD PARASITISM AND ECTOPARASITE RICHNESS–SCALE‐DEPENDENT DIVERSITY INTERACTIONS IN A THREE‐LEVEL HOST–PARASITE SYSTEM

Brood parasitic birds, their foster species and their ectoparasites form a complex coevolving system composed of three hierarchical levels. However, effects of hosts’ brood parasitic life‐style on the evolution of their louse (Phthiraptera: Amblycera, Ischnocera) lineages have never been tested. We present two phylogenetic analyses of ectoparasite richness of brood parasitic clades. Our hypothesis was that brood parasitic life‐style affects louse richness negatively across all avian clades due to the lack of vertical transmission routes. Then, narrowing our scope to brood parasitic cuckoos, we explored macroevolutionary factors responsible for the variability of their louse richness. Our results show that taxonomic richness of lice is lower on brood parasitic clades than on their nonparasitic sister clades. However, we found a positive covariation between the richness of cuckoos’ Ischnoceran lice and the number of their foster species, possibly due to the complex and dynamic subpopulation structure of cuckoo species that utilize several host species. We documented diversity interactions across a three‐level host parasite system and we found evidence that brood parasitism has opposing effects on louse richness at two slightly differing macroevolutionary scales, namely the species richness and the genera richness.     

Differential visual ornamentation between brood parasitic and parental cuckoos

The evolution of brood parasitism should affect adult phenotypic traits due to sexual selection as well as the parasite–host interactions, although it is rarely focused on. Sexual selection theory predicts extravagant secondary sexual characteristics in brood parasites whereas immature‐like modest sexual characteristics in parental species. This is because juvenile‐like immature traits can attract mates by exploiting parental care for young (i.e. attraction to young), and because the good parent process, which favours traits that signal parental care ability, would constrain the evolution of costly secondary sexual characteristics due to evolutionary trade‐offs between parental investment and sexually selected traits. Using a phylogenetic comparative approach, we studied plumage and bare‐part characteristics of adults in relation to brood parasitism in cuckoos (family Cuculidae), in which brood parasitism together with loss of parental care has evolved three times. As predicted, we found that nonparasitic cuckoos had plumage more similar to the juveniles than did brood parasitic cuckoos. Furthermore, nonparasitic cuckoos had a higher probability of having additional bare skin, that is a seemingly less costly, hatchling‐like trait, than did brood parasitic cuckoos. This finding further supports the link between parental care and sexual selection, although the influence of a parasite–host interaction cannot be excluded. The analysis of evolutionary pathways suggested interdependent evolution of additional bare skin and brood parasitism. Brood parasitism together with the loss of parental care may prevent the maintenance of a modest phenotype similar to the young, and vice versa in some cases.     

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.     

Differences in intestinal microbiota between avian brood parasites and their hosts

The intestinal microbiota determines the effectiveness of digestion in vertebrates, and is influenced by the external environment (mainly the diet), gut characteristics, and phylogeny. Avian brood-parasitic nestlings of the sub-family Cuculinae develop in nests of phylogenetically distant passerines and can be fed with the host diet. If the shaping of bacterial communities is dominated by phylogenetic constraints, and therefore the microbiota of parasitic nestlings differs from that of host nestlings, the energy and micronutrients that parasites and hosts obtain from a similar amount of food would be different. In this case, the bacterial communities of parasitic and host nestlings would have important consequences with respect to brood parasite development. By experimentally creating mixed broods of magpies ( Pica pica ) and great spotted cuckoos ( Clamator glandarius ), we investigated their cloacal microbiota using ribosomal intergenic spacer analysis. We found significant differences in bacterial assemblages of the parasitic and host nestlings, although none of the phylotypes were specific in either great spotted cuckoos or magpies. Cuckoos presented more complex communities, which could help the brood parasitic life style and allow the digestion of food provided by different potential hosts. Moreover, the intestinal morphology is different between the two species due to phylogenetic differences in the two taxa, which would influence the dissimilar bacterial assemblages. The detected differences in microbiota of great spotted cuckoo and magpie nestlings, which might occur in other brood parasite–host systems, may imply a lower digestion efficiency in parasites. Thus, the higher level requirements of cuckoo nestlings may be explained, at least in part, by cuckoos having a suboptimal bacterial community for processing the host diet.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 406–414.     

The gut microbiota of brood parasite and host nestlings reared within the same environment: disentangling genetic and environmental effects

Gut microbiota are essential for host health and survival, but we are still far from understanding the processes involved in shaping their composition and evolution. Controlled experimental work under lab conditions as well as human studies pointed at environmental factors (i.e., diet) as the main determinant of the microbiota with little evidence of genetic effects, while comparative interspecific studies detected significant phylogenetic effects. Different species, however, also differ in diet, feeding behavior, and environmental characteristics of habitats, all of which also vary interspecifically, and, therefore, can potentially explain most of the detected phylogenetic patterns. Here, we take advantage of the reproductive strategy of avian brood parasites and investigate gut microbiotas (esophageal (food and saliva) and intestinal) of great spotted cuckoo (Clamator glandarius) and magpie (Pica pica) nestlings that grow in the same nests. We also estimated diet received by each nestling and explored its association with gut microbiota characteristics. Although esophageal microbiota of magpies and great spotted cuckoos raised within the same environment (nest) did not vary, the microbiota of cloacal samples showed clear interspecific differences. Moreover, diet of great spotted cuckoo and magpie nestlings explained the microbiota composition of esophageal samples, but not of cloaca samples. These results strongly suggest a genetic component determining the intestinal microbiota of host and parasitic bird species, indicating that interspecific differences in gut morphology and physiology are responsible for such interspecific differences.Subject terms: Microbial ecology, Community ecology     

WHY DO PARASITIC CUCKOOS HAVE SMALL BRAINS? INSIGHTS FROM EVOLUTIONARY SEQUENCE ANALYSES

Brain size is under many opposing selection pressures. Estimating their relative influence and reconstructing the brain's evolutionary history have, however, proved difficult. Here, we confirm the suggestion that the brain of brood parasitic cuckoos is smaller in relation to their body weight than that of nonparasitic cuckoo species. Two hypotheses explaining reductions in brain size are tested, using phylogenetically controlled correlations and evolutionary pathway analyses. In a novel approach, the pathway models are combined to build the most likely evolutionary sequence of trait changes correlating with changes in brain size. Brain size changed before brood parasitism, followed by a shift toward less-productive habitats and an increase in migration. This sequence shows that brain size was not reduced as a consequence of a loss of cognitive skills related to chick provisioning, and it offers no support for the hypothesis that an increase in energetic demands or a reduction in energy availability selected for a reduction of brain size. Instead, the sequence suggests that the reduction in energetic demands due to the smaller brain size and parasitic breeding strategy may have enabled parasitic cuckoos to colonize new niches.     

Striking difference in response to expanding brood parasites by birds in western and eastern Beringia

Two species of obligate brood‐parasitic Cuculus cuckoos are expanding their ranges in Beringia. Both now breed on the Asian side, close to the Bering Strait, and are found in Alaska during the breeding season. From May to July 2017, we used painted 3D‐printed model eggs of two cuckoo host‐races breeding in northeastern Siberia to test behavioral responses of native songbirds on both sides of the Bering Strait, with particular attention to species that are known cuckoo hosts in their Siberian range. Each host nest was tested after the second egg was laid and, if possible, again 4 days later with a model of a different type. Although our Siberian study site was also outside the known breeding ranges of the cuckoos, we found that Siberian birds had strong anti‐parasite responses, with 14 of 22 models rejected. In contrast, birds in Alaska had virtually no detectable anti‐parasite behaviors, with only one of 96 models rejected; the rejecters were Red‐throated Pipits (Anthus cervinus). Such differences suggest that the cuckoos might successfully parasitize naïve hosts and become established in North America whether or not their historic host species are widely available.     

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.     

Hawk mimicry in cuckoos and anti‐parasitic aggressive behavior of barn swallows in Denmark and China

Hosts of brood parasites defend their nests against parasitism by aggression and subsequently, if parasitized, by rejection of the parasite egg or nestling. Cuckoos have evolved plumage mimicry with convergence towards the phenotype of Accipiter hawks that are common predators of cuckoo hosts. Here we tested two alternative hypotheses 1) whether barn swallows Hirundo rustica have evolved less aggressive behavior towards cuckoos in areas of sympatry with more abundant Accipiter hawks; and 2) whether barn swallows have evolved more aggressive anti‐parasite behavior in areas with a single species of cuckoo. We presented dummies of common cuckoo Cuculus canorus, sparrowhawk Accipiter nisus and Oriental turtledove Streptopelia orientalis (a benign control) at the nests of barn swallows during breeding, while recording intensity of response and proximity of barn swallows to the dummy. We demonstrated that cuckoos moved away when attacked aggressively and approached more closely by barn swallows showing that barn swallow behavior was efficient at driving away cuckoos. Barn swallows were significantly more aggressive and approached cuckoo and sparrowhawk dummies more closely in Denmark than in China, despite sparrowhawks being relatively more common in Denmark. Responses towards cuckoo dummies differed from responses towards sparrowhawk dummies, showing that barn swallows distinguished between the two different causes of danger. These findings are inconsistent with a less aggressive response towards cuckoo dummies in areas of sympatry with more abundant Accipiter hawks, but consistent with the alternative hypothesis that barn swallows have evolved more aggressive behavior towards cuckoos in areas with a single species of brood parasite, but not in areas with multiple species of parasites, where it is harder for hosts to tell the difference.     

Does coevolution promote species richness in parasitic cuckoos?

Why some lineages have diversified into larger numbers of species than others is a fundamental but still relatively poorly understood aspect of the evolutionary process. Coevolution has been recognized as a potentially important engine of speciation, but has rarely been tested in a comparative framework. We use a comparative approach based on a complete phylogeny of all living cuckoos to test whether parasite–host coevolution is associated with patterns of cuckoo species richness. There are no clear differences between parental and parasitic cuckoos in the number of species per genus. However, a cladogenesis test shows that brood parasitism is associated with both significantly higher speciation and extinction rates. Furthermore, subspecies diversification rate estimates were over twice as high in parasitic cuckoos as in parental cuckoos. Among parasitic cuckoos, there is marked variation in the severity of the detrimental effects on host fitness; chicks of some cuckoo species are raised alongside the young of the host and others are more virulent, with the cuckoo chick ejecting or killing the eggs/young of the host. We show that cuckoos with a more virulent parasitic strategy have more recognized subspecies. In addition, cuckoo species with more recognized subspecies have more hosts. These results hold after controlling for confounding geographical effects such as range size and isolation in archipelagos. Although the power of our analyses is limited by the fact that brood parasitism evolved independently only three times in cuckoos, our results suggest that coevolutionary arms races with hosts have contributed to higher speciation and extinction rates in parasitic cuckoos.     

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.     

Chemical defence in avian brood parasites: production and function of repulsive secretions in common cuckoo chicks

The use of active chemical defence against predators is relatively rare in birds. Among others, it has been reported for some members of family Cuculidae whose chicks, when threatened, expel dark foul‐smelling liquid from their cloaca. Apart from the brood parasitic great spotted cuckoo Clamator glandarius, however, this phenomenon has not yet been systematically studied in any other cuckoo species. Here we investigated the repellent behaviour in the evicting brood parasite, the common cuckoo Cuculus canorus, parasitizing the great reed warbler Acrocephalus arundinaceus. We explored whether production of secretions varies with chick age or size, and tested its presumed repellent function against various types of predators. We found that the production of secretions commenced at the age of approximately eight days, then gradually increased and decreased again shortly before fledging. Furthermore, we experimentally confirmed a more intensive repellent effect of the secretions on mammal predators than on avian predators, such as raptors and owls. The secretions have, however, no effect on corvid predators, probably because these scavengers often consume malodorous food. Further experimental studies together with phylogenetic comparative analyses are needed to elucidate the origin and function of this intriguing phenomenon both in parasitic and non‐parasitic cuckoos.     

大杜鹃对家燕的巢寄生

了解杜鹃(Cuculus spp.)对不同宿主鸟类的巢寄生,是研究杜鹃与其宿主之间协同进化的重要基础资料。大杜鹃(Cuculus canorus)和家燕(Hirundo rustica)分布遍及全国,且为同域分布,但两者之间的寄生现象尚未有过系统调查。2012年和2014年4~8月,对繁殖于吉林市昌邑区桦皮厂镇(34°58′44.18″N,126°13′26.83″E,海拔184 m)和海南岛的家燕种群进行调查,结果表明,吉林市昌邑区桦皮厂镇家燕种群的寄生率为2.4%(1/42),而在海南岛所调查的1 719个家燕巢未发现杜鹃寄生现象。同时在网络上搜集家燕巢寄生的报道案例,共记录到13巢家燕被大杜鹃寄生繁殖,均发生在北方的家燕种群。     

Coevolution is linked with phenotypic diversification but not speciation in avian brood parasites

Coevolution is often invoked as an engine of biological diversity. Avian brood parasites and their hosts provide one of the best-known examples of coevolution. Brood parasites lay their eggs in the nests of other species, selecting for host defences and reciprocal counteradaptations in parasites. In theory, this arms race should promote increased rates of speciation and phenotypic evolution. Here, we use recently developed methods to test whether the three largest avian brood parasitic lineages show changes in rates of phenotypic diversity and speciation relative to non-parasitic lineages. Our results challenge the accepted paradigm, and show that there is little consistent evidence that lineages of brood parasites have higher speciation or extinction rates than non-parasitic species. However, we provide the first evidence that the evolution of brood parasitic behaviour may affect rates of evolution in morphological traits associated with parasitism. Specifically, egg size and the colour and pattern of plumage have evolved up to nine times faster in parasitic than in non-parasitic cuckoos. Moreover, cuckoo clades of parasitic species that are sympatric (and share similar host genera) exhibit higher rates of phenotypic evolution. This supports the idea that competition for hosts may be linked to the high phenotypic diversity found in parasitic cuckoos.     

Internal incubation and early hatching in brood parasitic birds

The offspring of brood parasitic birds benefit from hatching earlier than host young. A proposed but little-known strategy to achieve this is 'internal incubation', by retaining the egg in the oviduct for an additional 24 h. To test this, we quantified the stage of embryo development at laying in four brood parasitic birds (European cuckoo, Cuculus canorus; African cuckoo, Cuculus gularis; greater honeyguide, Indicator indicator; and the cuckoo finch, Anomalospiza imberbis). For the two cuckoos and the honeyguide, all of which lay at 48 h intervals, embryos were at a relatively advanced stage at laying; but for the cuckoo finch (laying interval: 24 h) embryo stage was similar to all other passerines laying at 24 h intervals. The stage of embryo development in the two cuckoos and honeyguide was similar to that of a non-parasitic species that lay at an interval of 44-46 h, but also to the eggs of the zebra finch Taeniopygia guttata incubated artificially at body temperature immediately after laying, for a further 24 h. Comparison with the zebra finch shows that internal incubation in the two cuckoos and honeyguide advances hatching by 31 h, a figure consistent with the difference between the expected and the observed duration of incubation in the European cuckoo predicted from egg mass. Rather than being a specific adaptation to brood parasitism, internal incubation is a direct consequence of a protracted interval between ovulation (and fertilization) and laying, but because it results in early hatching may have predisposed certain species to become brood parasitic.     

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.     

Egg color variation,but not egg rejection behavior,changes in a cuckoo host breeding in the absence of brood parasitism

Interactions between parasitic cuckoos and their songbird hosts form a classical reciprocal “arms race,” and are an excellent model for understanding the process of coevolution. Changes in host egg coloration via the evolution of interclutch variation in egg color or intraclutch consistency in egg color are hypothesized counter adaptations that facilitate egg recognition and thus limit brood parasitism. Whether these antiparasitism strategies are maintained when the selective pressure of parasitism is relaxed remains debated. However, introduced species provide unique opportunities for testing the direction and extent of natural selection on phenotypic trait maintenance and variation. Here, we investigated egg rejection behavior and egg color polymorphism in the red‐billed leiothrix (Leiothrix lutea), a common cuckoo (Cuculus canorus) host, in a population introduced to Hawaii 100 years ago (breeding without cuckoos) and a native population in China (breeding with cuckoos). We found that egg rejection ability was equally strong in both the native and the introduced populations, but levels of interclutch variation and intraclutch consistency in egg color in the native population were higher than in the introduced population. This suggests that egg rejection behavior in hosts can be maintained in the absence of brood parasitism and that egg appearance is maintained by natural selection as a counter adaptation to brood parasitism. This study provides rare evidence that host antiparasitism strategies can change under parasite‐relaxed conditions and reduced selection pressure.     

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.     

Competition with a host nestling for parental provisioning imposes recoverable costs on parasitic cuckoo chick's growth

Chicks of the brood parasitic common cuckoo (Cuculus canorus) typically monopolize host parental care by evicting all eggs and nestmates from the nest. To assess the benefits of parasitic eviction behaviour throughout the full nestling period, we generated mixed broods of one cuckoo and one great reed warbler (Acrocephalus arundinaceus) to study how hosts divide care between own and parasitic young. We also recorded parental provisioning behaviour at nests of singleton host nestlings or singleton cuckoo chicks. Host parents fed the three types of broods with similar-sized food items. The mass of the cuckoo chicks was significantly reduced in mixed broods relative to singleton cuckoos. Yet, after the host chick fledged from mixed broods, at about 10-12 days, cuckoo chicks in mixed broods grew faster and appeared to have compensated for the growth costs of prior cohabitation by fledging at similar weights and ages compared to singleton cuckoo chicks. These results are contrary to suggestions that chick competition in mixed broods of cuckoos and hosts causes an irrecoverable cost for the developing brood parasite. Flexibility in cuckoos' growth dynamics may provide a general benefit to ecological uncertainty regarding the realized successes, failures, and costs of nestmate eviction strategies of brood parasites.     

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.