The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites

There is considerable variation in rejection rates of parasitic eggs among hosts of avian brood parasites. In this article, we develop a model that can be used to predict host egg rejection behavior in brood parasite-host systems in general, by considering both intra- and interclutch variation in host egg appearance; clutch characteristics that may be important in calculating the fitness of individuals adopting rejecter or acceptor strategies. In addition, we consider the importance of learning the appearance of own eggs during the first breeding attempt and host probability of survival between breeding seasons on evolution of rejection behavior. Based on this model we can predict at which level of parasitism fitness of rejecter individuals is higher than that of acceptor individuals and vice versa. The model analyses show that variation in egg appearance can be a key factor for the evolution of host defense against parasitism. In more detail, analyses show that we should expect to find a prolonged learning period only in hosts that have a high intraclutch variation in egg appearance, because such hosts may potentially experience high costs in terms of recognition errors. Furthermore, learning is in general more adaptive in parasite-host systems in which hosts do have some reproductive success even when parasitized, and when parasitism rates are moderate. By including variables that have not been considered in previous models, our model represents a useful tool in investigations of host rejection behavior in various host-parasite systems.     

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.     

Brood parasite eggs enhance egg survivorship in a multiply parasitized host

Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests. We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this 'dilution effect', comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection.     

Evolution of defences against cuckoo (<Emphasis Type="Italic">Cuculus canorus</Emphasis>) parasitism in bramblings (<Emphasis Type="Italic">Fringilla montifringilla</Emphasis>): a comparison of four populations in Fennoscandia

The brood parasitic common cuckoo Cuculus canorus has a history of coevolution that involves numerous passerine hosts, but today only a subset is known to be regularly parasitised in any area. In some hosts, there is significant variation in the occurrence of parasitism between populations, but still individuals in non-parasitised populations show strong antiparasite defences. In the present study we compared the strength of egg rejection of four distant Fennoscandian brambling Fringilla montifringilla populations experiencing different levels of cuckoo parasitism (0–6%). Egg rejection ability was in general very well developed and we did not find any population differences in the relationship between egg rejection probability and similarity between host and experimental parasitic eggs. Furthermore, bramblings very rarely made errors in rejection, indicating that selection against rejection behaviour is likely to be very weak. The brambling-cuckoo system therefore differs from other well studied systems which are characterised by pronounced spatial and temporal variation in the host’s level of defence. This result is unlikely to reflect independent replication of the same evolutionary trajectory because the weak breeding site tenacity of bramblings should result in an extreme amount of gene flow within the distribution area and thus strongly impede localised responses to selection. Instead, lack of geographic variation has more likely arisen because bramblings respond to selection as one evolutionary unit, and because the average parasitism pressures have been high enough in the past to cause regional fixation of rejection alleles and evolution of clutch characteristics that facilitate cost free egg recognition.     

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.     

REED WARBLER HOSTS FINE‐TUNE THEIR DEFENSES TO TRACK THREE DECADES OF CUCKOO DECLINE

Interactions between avian hosts and brood parasites can provide a model for how animals adapt to a changing world. Reed warbler (Acrocephalus scirpaceus) hosts employ costly defenses to combat parasitism by common cuckoos (Cuculus canorus). During the past three decades cuckoos have declined markedly across England, reducing parasitism at our study site (Wicken Fen) from 24% of reed warbler nests in 1985 to 1% in 2012. Here we show with experiments that host mobbing and egg rejection defenses have tracked this decline in local parasitism risk: the proportion of reed warbler pairs mobbing adult cuckoos (assessed by responses to cuckoo mounts and models) has declined from 90% to 38%, and the proportion rejecting nonmimetic cuckoo eggs (assessed by responses to model eggs) has declined from 61% to 11%. This is despite no change in response to other nest enemies or mimetic model eggs. Individual variation in both defenses is predicted by parasitism risk during the host's egg‐laying period. Furthermore, the response of our study population to temporal variation in parasitism risk can also explain spatial variation in egg rejection behavior in other populations across Europe. We suggest that spatial and temporal variation in parasitism risk has led to the evolution of plasticity in reed warbler defenses.     

Cuckoos versus reed warblers: Adaptations and counteradaptations

At study sites in Cambridgeshire, England, the percentage of reed warbler, Acrocephalus scirpaceus, nests parasitized by cuckoos, Cuculus canorus, in 2 years was 22·5% and 9·1%. The warblers rejected cuckoo eggs at 19% of parasitized nests. Parasitized clutches suffered less predation than unparasitized clutches, suggesting that the cuckoo itself was the major predator, plundering nests too advanced for parasitism so that the hosts would re-lay. The cuckoos laid a mimetic egg, parasitized nests in the afternoons during the host laying period, usually removed one host egg, laid a remarkably small egg and laid very quickly. Nests were experimentally parasitized with model eggs to study the significance of this procedure. Experiments showed that host discrimination selects for: (1) egg mimicry by cuckoos (poorer matching model eggs were more likely to be rejected); (2) parasitism during the laying period (mimetic eggs put in nests before host laying began were rejected); (3) afternoon laying (mimetic eggs were less likely to be accepted in the early morning than in the afternoon, when hosts were more often absent from the nest); (4) a small egg (large eggs, typical of non-parasitic cuckoos, were more likely to be rejected); (5) rapid laying (a stuffed cuckoo on the nest stimulated increased rejection of model eggs), and (6) sets a limit to host egg removal by cuckoos (if more than one or two are removed desertion may occur). Mimicry may also be selected for because it reduced the chance that second cuckoos can discriminate the first cuckoo's egg from the host's clutch. Predation did not select for mimicry; nests with a non-mimetic egg did not suffer greater predation than those with a mimetic egg. Host rejection of model eggs did not depend on: (1) stage of parasitism once host egg laying had begun (nevertheless cuckoos were more likely to lay early in the host laying period probably to increase the chance the cuckoo chick hatched); (2) removal of a host egg (however, this reduced the incidence of unhatched eggs so cuckoos may remove a host egg so as not to exceed the host incubation limit). There were two costs of rejection, an ‘ejection’ cost (own eggs ejected as well as the cuckoo egg) and, with mimetic eggs, a ‘recognition’ cost (own eggs ejected instead of the cuckoo egg). Reed warblers did not discriminate against unlike chicks (another species) and did not favour either a cuckoo chick or their own chicks when these were placed in two nests side by side. Possible reasons why the hosts discriminate against unlike eggs but not unlike chicks are discussed.     

Attractive blue‐green egg coloration and cuckoo−host coevolution

Recent evidence suggests that blue‐green coloration of bird eggshells may be related to female and/or egg phenotypic quality, and that such colour may affect parental effort and therefore the nutritional environment of developing nestlings. Here we suggest that these relationships and the signal function of eggshell coloration would affect the outcome of coevolution between avian brood parasites and their hosts in at least three different non‐exclusive evolutionary pathways. First, by laying blue‐green coloured eggs, cuckoo females may exploit possible sensory biases of their hosts, constraining the evolution of parasitic egg recognition, and thus avoid rejection. Second, because of the relatively high costs of laying blue eggs, cuckoo females may be limited in their ability to mimic costly blue‐green eggs of their hosts because cuckoo females lay many more eggs than their hosts. Furthermore, costs associated with foreign egg recognition errors would be relatively higher for hosts laying blue eggs. Third, cuckoos may use coloration of host eggs for selecting individuals or specific hosts of appropriate phenotypic quality (i.e. parental abilities). We here explored some predictions emerging from the above scenarios and found partial support for two of them by studying egg coloration of European cuckoos (Cuculus canorus) and that of their 25 main hosts, as well as parasitism and rejection rate of hosts. Cuckoo hosts parasitized with more blue, green, and ultraviolet cuckoo eggs, or those laying more blue‐green eggs, were more prone to accept experimental parasitism with artificial cuckoo eggs. In addition, coloration of cuckoo eggs is more variable when parasitizing hosts laying bluer‐greener eggs, even after controlling for the effect of host egg coloration (i.e. degree of egg matching). Globally, our results are consistent with the proposed hypothesis that host egg traits that are related to phenotypic quality of hosts, such as egg coloration, may have important implications for the coevolutionary interaction between hosts and brood parasites. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 154–168.     

Rejection of artificial cuckoo (Cuculus canorus) eggs in relation to variation in egg appearance among reed warblers (Acrocephalus scirpaceus)

Passerines that are exposed to brood parasitism can evolve reduced intraclutch variation in egg appearance to facilitate recognition and rejection of the parasitic egg. This has been shown to be true for European passerine species that are assumed to have participated in an evolutionary arms race with the cuckoo (Cuculus canorus). However, few investigations have been carried out with the aim of finding out whether there is a relationship between these two traits within a species. In this study, we compare the level of intraclutch variation in egg appearance and the rejection of an unlike parasitic egg within a population of reed warblers (Acrocephalus scirpaceus) in the south-eastern part of the Czech Republic. We parasitized reed warbler nests with an artificial non-mimetic cuckoo egg, and then monitored the reaction of the hosts. In 27 out of 48 nests (56.3%) the parasitic egg was rejected. The rejecter pairs had a statistically significantly lower intraclutch variation in egg appearance than the acceptor pairs. We discuss possible explanations for the observed relationship between rejection of unlike eggs and intraclutch variation in egg appearance within this population of reed warblers. The results are consistent with the evolutionary arms race hypothesis, but the intermediate rejection rate found in this population could also be maintained by an equilibrium between acceptors and rejecters due to rejection costs.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

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.     

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.     

Experimental Manipulation of Intraclutch Variation in the Great Reed Warbler Shows No Effect on Rejection of Parasitic Eggs

In the continuing arms race between hosts and brood parasites, hosts are expected to reduce variation in the appearance of their own eggs within clutches, as it facilitates recognition of parasitic eggs. At the same time, by increasing interclutch variation, hosts should make it more difficult for parasites to evolve perfectly mimetic eggs. In this study, we experimentally manipulated intraclutch variation in the great reed warbler, Acrocephalus arundinaceus, in Hungary, where this species is heavily (c. 64%) parasitized by the common cuckoo, Cuculus canorus. We placed artificial cuckoo eggs, which appeared moderately mimetic to humans, in two groups of nests; in one group we increased variability of egg appearance within clutches by exchanging host eggs among nests. These clutches showed a significantly higher intraclutch variability than natural clutches, which we used as a control group. Our results indicate that it has no effect on rejection behaviour in this species, neither when variation was increased experimentally, nor within the natural range of variation displayed by our population. We suggest that when parasitism is high, selection for reduced intraclutch variation may be less important than frequency‐dependent selection for increased variation between individuals within a host population.     

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.     

Rapid increase of host defence against brood parasites in a recently parasitized area: the case of village weavers in Hispaniola

Passerine hosts of brood parasitic birds usually vary in their ability to discriminate and reject alien eggs. Two main hypotheses have been suggested to explain the persistence of acceptor individuals in species that are exploited by brood parasites. The evolutionary lag hypothesis postulates that some hosts have not yet evolved the ability to discriminate against alien eggs. Once the ability to recognize the parasitic egg has appeared by mutation, it spreads because of the selective advantage of rejection. Parasites are then selected to produce more mimetic eggs, in order to escape host discrimination, which eventually ends up in an arms race between the parasite and the host. The evolutionary equilibrium hypothesis is based on the assumption that rejection behaviour is costly in the absence of parasitism, because of recognition errors. Acceptor hosts can persist when parasitism rate fluctuates or is consistently low. Indirect evidence for costs of rejection in the absence of parasitism has been provided by Cruz and Wiley, who reported low rejection rate for a population of village weavers (Ploceus cucullatus) introduced from Africa to Hispaniola (West Indies) more than a century ago. In Africa the species is parasitized by Chrysococcyx cuckoos and shows high levels of egg discrimination. Since no brood parasite was present in Hispaniola, Cruz and Wiley suggested that rejection was selected against in the absence of parasitism due to recognition costs. Introduction of village weavers in Hispaniola, therefore, provided a unique opportunity to test the decline of an adaptation. During the past century the shiny cowbird (Molothrus bonariensis) has expanded its range-invading most of the West Indies from South America. It was first observed in Hispaniola in 1972, and it started to exploit village weavers as a host. Given that shiny cowbirds substantially reduce the reproductive success of weavers, we should expect higher rejection rates nowadays compared to those reported by Cruz and Wiley 16 years ago. In agreement with this prediction, we found a high rejection rate of cowbird model eggs (89.3%, 95% CI = 81.1 to 97.5%), moderate levels of rejection of non-mimetic weaver model eggs (67.5%, 95% CI = 52.5 to 82.5%) and rather low levels of rejection of mimetic weaver model eggs (25%, 95% CI = 4 to 46%). The rejection rate of artificial cowbird eggs has therefore increased from 13.8% (95% CI = 5 to 22.6%) to 89.3% in 16 years. To check whether this rapid increase in host resistance is compatible with a genetic microevolutionary change, we built a population dynamics model where, as an upper bound, resistance is inherited by the progeny with a probability of one. This simple model shows that observed changes of rejection rate are compatible with a genetic microevolutionary shift only under the most favourable scenario for rejecters to spread. Relaxing one or several of these assumptions (e.g. high parasitism rate, absence of rejection costs) considerably lengthens the period needed for rejecters to spread. We suggest that both genetic and learning processes might be involved in the observed changes.     

Getting rid of the cuckoo Cuculus canorus egg: why do hosts delay rejection?

Egg discrimination is well documented in many hosts of avianbrood parasites, but the proximate mechanisms of egg recognitionand rejection decisions are poorly understood. Relevant in thisrespect is the observation that rejectors of parasite eggs oftendelay their response. This delay has implications for understandingmechanisms important for egg recognition and is the main focusof the present study. We investigated experimentally the relativeeffects of egg mimicry and eggshell strength of common cuckooCuculus canorus eggs on the delay in rejection in marsh warblersAcrocephalus palustris. In addition, by video recording hostresponses, we elucidate the proximate mechanisms behind thedelayed rejections. Host nests were experimentally parasitizedwith 3 types of real eggs differing in mimicry and/or eggshellstrength. Both egg mimicry and eggshell strength significantlyaffected the time to rejection, but the effect of mimicry wasdominant. The delayed rejection of mimetic eggs was explainedby the existence of latency to the release of rejection behaviorbecause of recognition problems. Second, when rejection responsetowards mimetic eggs was initiated, it was less intense comparedwith hosts experiencing nonmimetic eggs. Our results are consistentwith the hypothesis that host motivation when confronted withmimetic eggs needs to increase above a certain threshold beforerejection behavior is released, which likely minimizes the riskof recognition errors. An additional component of the delayin rejection as shown by hosts facing nonmimetic eggs was theseemingly inefficient host rejection behavior, probably reflectinglack of previous experience.     

Egg rejection and clutch phenotype variation in the plain prinia Prinia inornata

Avian hosts of brood parasites can evolve anti‐parasitic defenses to recognize and reject foreign eggs from their nests. Theory predicts that higher inter‐clutch and lower intra‐clutch variation in egg appearance facilitates hosts to detect parasitic eggs as egg‐rejection mainly depends on the appearance of the egg. Therefore, we predict that egg patterns and rejection rates will differ when hosts face different intensity of cuckoo parasitism. We tested this prediction in two populations of the plain prinia Prinia inornata: Guangxi in mainland China with high diversity and density of cuckoo species, and Taiwan where there is only one breeding cuckoo species, the oriental cuckoo Cuculus optatus. As expected, egg patterns were similar within clutches but different among clutches (polymorphic eggs) in the mainland population, while the island population produced more uniform egg morphs. Furthermore, the mainland population showed a high rate of egg rejection, while the island population exhibited dramatically reduced egg grasp‐rejection ability in the absence of parasitism by the common cuckoo Cuculus canorus. Our study suggests that prinias show lower intra‐clutch consistency in egg colour and lose egg‐rejecting ability under relaxed selection pressure from brood parasitism.     

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.     

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.     

Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds

Many passerine host species have counteracted the parasite egg mimicry in their coevolutionary arms race with the common cuckoo (Cuculus canorus) by evolving increased interclutch and reduced intraclutch variation in egg appearance. Such variations make it easier for hosts to recognize a foreign egg, reduce the possibility of making recognition errors, and reduce the ability of the cuckoo to mimic the eggs of a particular host. Here, we investigate if such clutch characteristics have evolved among North American passerines. We predict that due to the absence of brood parasites with egg mimicry on this continent, these passerines should (1) not show any relationship between rejection rates and intra- or interclutch variation, and (2) intraclutch variation should be lower and interclutch variation higher in European hosts exposed to cuckoo parasitism as compared to North American hosts parasitized by cowbirds. Here we present data that show support for most of these and other predictions, as well as when controlling statistically for effects of common descent. However, the effect of continent on intraclutch variation was less than predicted and we discuss a possible reason for this. All things considered, the results demonstrate that parasitism by a specialist brood parasite with egg mimicry is a powerful selective force regarding the evolution of egg characteristics in passerine birds.