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.     

An investigation into egg-acceptance by azure-winged magpies and host-recognition by great spotted cuckoo chicks

Tests using magpie's eggs (which are very similar to those of the great spotted cuckoo) on azure-winged magpies (Cyanopica cyanea) showed that the latter accept strange eggs, rejecting only 25% of them. We therefore suggest that they are an accepter species, and as such a substitute host species for the great spotted cuckoo (Clamator glandarius). We suggest a theory for the transition from ‘Accepter Species’ to ‘Non-mimetic-egg Rejecter Species’ by hosts of specialist brood parasites. We have obtained evidence of host recognition by great spotted cuckoo chicks of typical or atypical host species characteristics. Basing our theory on the calls of parasitic chicks reared in the nests of the azure-winged magpies and magpies (Pica pica), we suggest that the foregoing is the mating mechanism necessary for the parasitization of a new host species.     

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.     

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.     

Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos

Hosts may use two different strategies to ameliorate negative effects of a given parasite burden: resistance or tolerance. Although both resistance and tolerance of parasitism should evolve as a consequence of selection pressures owing to parasitism, the study of evolutionary patterns of tolerance has traditionally been neglected by animal biologists. Here, we explore geographical covariation between tolerance of magpies (Pica pica) and brood parasitism by the great spotted cuckoo (Clamator glandarius) in nine different sympatric populations. We estimated tolerance as the slope of the regression of number of magpie fledglings (i.e. host fitness) on number of cuckoo eggs laid in non-depredated nests (which broadly equals parasite burden). We also estimated prevalence of parasitism and level of host resistance (i.e. rejection rates of mimetic model eggs) in these nine populations. In accordance with the hypothetical role of tolerance in the coevolutionary process between magpies and cuckoos we found geographical variation in tolerance estimates that positively covaried with prevalence of parasitism. Levels of resistance and tolerance were not associated, possibly suggesting the lack of a trade-off between the two kinds of defences against great spotted cuckoo parasitism for magpies. We discuss the results in the framework of a mosaic of coevolutionary interactions along the geographical distribution of magpies and great spotted cuckoos for which we found evidence that tolerance plays a major role.     

Great Spotted Cuckoos Frequently Lay Their Eggs While Their Magpie Host is Incubating

Species that suffer from brood parasitism face a considerable reduction in their fitness which selects for the evolution of host defences. To prevent parasitism, hosts can mob or attack brood parasites when they approach the host nest and block the access to the nest by sitting on the clutch. In turn, as a counter‐adaptation, brood parasites evolved secretive behaviours near their host nests. Here, we have studied great spotted cuckoo (Clamator glandarius) egg‐laying behaviour and defence by their magpie (Pica pica) hosts inside the nest using continuous video recordings. We have found several surprising results that contradict some general assumptions. The most important is that most (71%) of the parasitic events by cuckoo females are completed while the magpie females are incubating. By staying in the nest, magpies force cuckoo females to lay their egg facing the high risk of being attacked by the incubating magpie (attack occurred in all but one of the events, n = 15). During these attacks, magpies pecked the cuckoo violently, but could never effectively avoid parasitism. These novel observations expand the sequence of adaptations and counter‐adaptations in the arms race between brood parasites and their hosts during the pre‐laying and laying periods.     

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.     

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

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

Rejection of parasitic eggs in relation to egg appearance in magpies

The coevolutionary process between avian brood parasites and their hosts predicts that low intraclutch variation in egg colour appearance favours egg discrimination of parasite eggs by hosts. Low intraclutch variation would also result in high interclutch variation, which would increase the difficulty of evolution of mimicry by the cuckoo, because many host colour patterns might coexist in the same host population. We explored this possibility using an experimental approach in the common magpie, Pica pica, and great spotted cuckoo, Clamator glandarius, system. We artificially parasitized magpie nests with great spotted cuckoo model eggs to assess host response in two populations in Spain (Guadix and Doñana) in relation to intraclutch variation in egg appearance, measured by ultraviolet-visible reflectance spectrophotometry. Individuals that rejected model cuckoo eggs had higher intraclutch variation than accepters, suggesting that an increase, rather than a decrease, in intraclutch variation in magpie egg appearance was advantageous for cuckoo egg discrimination.     

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.     

Ultraviolet reflectance of great spotted cuckoo eggs and egg discrimination by magpies

Hosts of obligate avian brood parasites use visual cues to distinguishbetween their own eggs and those of the parasite. Despite majordifferences between human and bird vision, most previous studieson cuckoo egg mimicry estimated color matching based on humancolor vision. Undetected by humans, ultraviolet reflectance(UVR) may play a previously ignored role for rejection behaviorin avian brood parasite systems. We explored this possibilityby manipulating UVR of great spotted cuckoo Clamator glandariuseggs and assessing the response of magpie Pica pica hosts. Wecoated cuckoo eggs with an ultraviolet (UV) light blocker thatreduced UVR but left the human visible reflectance (400–700nm) unaltered. The first control treatment also coated the eggsbut did not alter their reflectance. A second control groupof cuckoo eggs was maintained uncoated to control for handlingeffects on magpie discrimination. We artificially parasitizeda third of a breeding magpie population with each type of experimentalegg and studied the rejection of cuckoo eggs. We failed to findsignificant differences between rejection rate of cuckoo eggswith and without reduced reflectance in the UV region. Our resultsindicate that artificial reduction of UVR of cuckoo eggs doesnot affect the probability of ejection by magpie hosts.     

Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism

In a coevolutionary arms race between an interspecific broodparasite and its host species, both are expected to evolveadaptations and counteradaptations. We studied egg discriminationin the Australian warbler (Acrocephalus australis). This speciesis currently not significantly parasitized by the seven speciesof cuckoo for which it is a suitable host. However, experimentalbrood parasitism in the warbler revealed a fine tuned egg discriminationresponse towards non-mimetic and conspecific eggs, the firstsuch evidence in an Australian passerine: (1) non-mimetic eggswere significantly more often rejected than conspecific eggs;(2) only non-mimetic dummy eggs were rejected selectively,whereas rejection of conspecific eggs entailed a rejectioncost; (3) replacement of a host's egg with a conspecific eggduring egg laying resulted in a significantly higher rejectionrate than after the day of clutch completion; (4) by contrast,rejection rate after addition of a conspecific egg was independentof nest stage; (5) conspecific eggs introduced into a clutchduring the egg laying period led to a significantly highernest desertion rate and a lower egg ejection rate than afterthe day of clutch completion; and (6) addition of a conspecificegg led to egg ejection while egg replacement with a conspecificegg led to nest desertion. The fact that this species respondsdifferentially toward different modes of artificial parasitismsuggests that its egg discrimination has evolved to minimizethe costs of rejection and parasitism. The ability to rejecthighly mimetic conspecific eggs may explain the current paucityof brood parasitism in this species. The significance of thisfor brood parasite-host coevolution is discussed.     

Are blackcaps current winners in the evolutionary struggle against the common cuckoo?

Blackcaps Sylvia atricapilla reject artificial cuckoo eggs, and their eggs vary little in appearance within clutches, whereas among clutches eggs vary considerably. Low variation within clutches facilitates discrimination of parasitic eggs, whereas high variation among clutches makes it harder for the cuckoo to mimic the eggs of a certain host species. These traits have most probably evolved as counteradaptations against brood parasitism by the common cuckoo Cuculus canorus, even though blackcaps are not regularly parasitised today. In this study, we investigated how fine-tuned the rejection of parasitic eggs is in this species by introducing three types of eggs into their nests: a real non-mimetic egg the approximate size of a cuckoo egg, an artificial mimetic egg the size of a cuckoo egg and a real conspecific egg. As the rejection frequency of both mimetic and non-mimetic artificial cuckoo eggs has been shown to be high in previous studies, the variation in rejection behaviour between individuals is low, indicating that most individuals within the population are able to reject parasitic eggs. Thus, we predict that (1) the intraclutch variation in egg appearance should be generally low in all individuals, and that (2) regarding conspecific eggs, rejection decisions should be highly dependent on the degree of mimicry between parasitic and host eggs. We found support for these predictions, which indicates that due to their highly sophisticated countermeasures against brood parasitism, blackcaps can probably be regarded as current winners of the arms race with the common cuckoo. Furthermore, the high and consistent rejection frequency of cuckoo eggs found throughout Europe for this species supports the spatial habitat structure hypothesis, which claims that woodland-nesting species breeding near trees, like blackcaps, presumably experienced a high level of parasitism throughout their range in the past and, therefore, their rejection behaviour, once evolved, spread rapidly to all populations.     

Great Spotted Cuckoo Fledglings Often Receive Feedings from Other Magpie Adults than Their Foster Parents: Which Magpies Accept to Feed Foreign Cuckoo Fledglings?

Natural selection penalizes individuals that provide costly parental care to non-relatives. However, feedings to brood-parasitic fledglings by individuals other than their foster parents, although anecdotic, have been commonly observed, also in the great spotted cuckoo (Clamator glandarius) – magpie (Pica pica) system, but this behaviour has never been studied in depth. In a first experiment, we here show that great spotted cuckoo fledglings that were translocated to a distant territory managed to survive. This implies that obtaining food from foreign magpies is a frequent and efficient strategy used by great spotted cuckoo fledglings. A second experiment, in which we presented a stuffed-cuckoo fledgling in magpie territories, showed that adult magpies caring for magpie fledglings responded aggressively in most of the trials and never tried to feed the stuffed cuckoo, whereas magpies that were caring for cuckoo fledglings reacted rarely with aggressive behavior and were sometimes disposed to feed the stuffed cuckoo. In a third experiment we observed feedings to post-fledgling cuckoos by marked adult magpies belonging to four different possibilities with respect to breeding status (i.e. composition of the brood: only cuckoos, only magpies, mixed, or failed breeding attempt). All non-parental feeding events to cuckoos were provided by magpies that were caring only for cuckoo fledglings. These results strongly support the conclusion that cuckoo fledglings that abandon their foster parents get fed by other adult magpies that are currently caring for other cuckoo fledglings. These findings are crucial to understand the co-evolutionary arms race between brood parasites and their hosts because they show that the presence of the host''s own nestlings for comparison is likely a key clue to favour the evolution of fledgling discrimination and provide new insights on several relevant points such as learning mechanisms and multiparasitism.     

Synchronization of laying by great spotted cuckoos and recognition ability of magpies

Brood parasites rely entirely on the parental care of host species to raise the parasitic nestlings until independence. The reproductive success of avian brood parasites depends on finding host nests at a suitable stage (i.e. during egg laying) for parasitism and weakly defensive (i.e. non‐ejector) hosts. Finding appropriate nests for parasitism may, however, vary depending on ecological conditions, including parasite abundance in the area, which also varies from one year to another and therefore may influence coevolutionary relationships between brood parasites and their hosts. In this scenario, we explored: 1) the degree of laying synchronization between great spotted cuckoos Clamator glandarius and magpies Pica pica during two breeding seasons, which varied in the level of selection pressure due to brood parasitism (i.e. parasitism rate); 2) magpie responses to natural parasitism in the pre‐laying period and successfulness of parasitic eggs laid at this stage; and 3) magpie responses to experimental parasitism performed at different breeding stages. We found that, during the year of higher parasitism rate, there was an increase in the percentage of parasitic eggs laid before magpies started laying. However, the synchronization of laying was poor both years regardless of the differences in the parasitism rate. The ejection rate was significantly higher during the pre‐egg‐laying and the post‐hatching stages than during the laying stage, and hatching success of parasitic eggs laid during the pre‐egg‐laying stage was zero. Thus, non‐synchronized parasitic eggs are wasted and therefore poor synchronization should be penalized by natural selection. We discuss four different hypotheses explaining poor synchronization.     

COMPARATIVE POPULATION STRUCTURE AND GENE FLOW OF A BROOD PARASITE,THE GREAT SPOTTED CUCKOO (CLAMATOR GLANDARIUS), AND ITS PRIMARY HOST,THE MAGPIE (PICA PICA)

The amount of gene flow is an important determinant of population structure and therefore of central importance for understanding coevolutionary processes. We used microsatellite markers to estimate population structure and gene flow rates of the great spotted cuckoo (Clamator glandarius) and its main host in Europe, the magpie (Pica pica), in a number of populations (seven and 15, respectively) across their distribution range in Europe. The genetic analysis shows that there exists a pattern of isolation by distance in both species, although the cuckoo data are only indicative due to a small sample size. Gene flow seems to be extensive between nearby populations, higher for magpies than cuckoos, and especially high for magpie populations within the area of distribution of the great spotted cuckoo. There is no correlation between genetic distances between magpie populations and genetic distances between cuckoo populations. We discuss the implications of extensive gene flow between magpie populations in sympatry with cuckoos for the population dynamics of hosts, in particular for the occurrence of egg rejection behavior in host populations and how the different rates of migration for both species can affect the dynamics of coevolutionary processes.     

Responses of great reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effects of a cuckoo Cuculus canorus dummy and egg mimicry

Egg rejection behaviour towards parasitic eggs was studied in a great reed warbler Acrocephalus arundinaceus population in central Hungary, which was heavily (about 65%) parasitised by the common cuckoo Cuculus canorus . Clutches were experimentally parasitised during the egg-laying period with artificial, moderately mimetic cuckoo eggs or with conspecific eggs that were good mimics of the hosts' eggs. Great reed warblers rejected 76.2% of the artificial cuckoo eggs, mainly by ejection, but accepted most of the conspecific eggs (87.5%). Cuckoo eggs in naturally parasitised clutches were rejected at a lower rate (32%). When, in addition to the egg mimicry experiments, a stuffed cuckoo was placed near the nest, accompanied by the recording of a female cuckoo call, hosts' rejection rate of the artificial cuckoo egg increased from 76% to 96%. The sight of the cuckoo, on the other hand, did not influence host's rejection behaviour when a conspecific egg was used in the experiment. A stuffed collared dove Streptopelia decaocto , accompanied by its call, was used as a control, and did not cause any increased rejection. Great reed warblers were more aggressive towards the cuckoo than to the dove dummy. When the cuckoo eggs in naturally parasitised clutches were exchanged with artificial cuckoo eggs, we observed no increase in the rejection rate. We conclude that great reed warblers in our heavily parasitised population are capable of detecting brood parasitism in their clutch by identifying the parasitic egg. The efficiency of this identification depends mainly on the mimicry of the foreign egg. The sight of the cuckoo at the nest may increase rejection rate by stimulus summation, and this conditional effect is mainly affected by the degree of mimicry of the parasitic egg.     

Great Spotted Cuckoo Nestlings but not Magpie Nestlings Starve in Experimental Age‐Matched Broods

Nestlings of non‐evicting avian brood‐parasites have to compete for food with foster parents' own nestlings. The outcome of these competitive contests is determined mainly by body size differences between parasitic and host nestlings. As part of the coevolutionary arms race between brood parasites and their hosts at the nestling stage, it has been reported that some host foster parents discriminate against parasitic chicks and are reluctant to feed them. Here, by experimentally creating size‐matched broods of different composition (only magpie Pica pica chicks, only great spotted cuckoo Clamator glandarius chicks or mixed broods), we show that great spotted cuckoo chicks starved in 20.2 per cent (17 of 84) of the parasitized magpie nests even in absence of size asymmetries, while in none (0 of 72) of the nests a magpie chick starved. As far as we know, this is the first record of non‐evictor brood parasitic nestlings starving without being smaller than their host nestmates in a frequently used host species. Nest composition had no effect on chick starvation. The cuckoo nestling starved even in two of the nests occupied by only one cuckoo chick. Our results could be explained by (1) magpies being reluctant to feed cuckoo chicks; (2) parasitic chicks receiving lower‐quality food items or cuckoo nestlings being sensitive to some particular component of the diet (e.g. cereal grains); and (3) the existence of cuckoo chick discrimination ability by magpie foster parents.     

GENETIC AND GEOGRAPHIC VARIATION IN REJECTION BEHAVIOR OF CUCKOO EGGS BY EUROPEAN MAGPIE POPULATIONS: AN EXPERIMENTAL TEST OF REJECTER-GENE FLOW

Host responses toward brood parasitism have been shown to differ among populations depending on the duration of sympatry between host and parasite, although populations not currently parasitized show rejection behavior against parasitic eggs. The persistence of rejection behavior in unparasitized host populations and rapid increases of rejection rate in parasitized ones have sometimes been explained as the result of gene flow of rejecter genes from sympatry to allopatry (rejecter-gene flow hypothesis). We present data on the rejection behavior of magpies (Pica pica) the main European host of the great spotted cuckoo (Clamator glandarius), in 15 populations (nine sympatric six allopatric) across their distribution range in Europe. Rejection rates of mimetic and nonmimetic model eggs were significantly higher in sympatric than in allopatric magpie populations, although differences in rejection rate of both mimetic and nonmimetic model eggs between magpie populations were significantly correlated even after controlling tor phylogenetic effects, with differences between sympatric and allopatric magpie populations being larger for mimetic than for nonmimetic model eggs. Differences in rejection of mimetic model eggs were related to both genetic and geographic distances between populations, but differences in rejection rate of nonmimetic model eggs were unrelated to these distances. However, when comparing only sympatric populations, differences in rejection rate of both mimetic and nonmimetic model eggs were related to geographic distances. A multiple autocorrelation analysis revealed that differences among populations in rejection rates of mimetic model eggs had a strong geographic component whereas the main component of rejection rate of nonmimetic model eggs was genetic rather than geographic. These results support the rejecter-gene flow hypothesis. We discuss differences in rejection rates of mimetic and nonmimetic model eggs that suggest the egg-recognition ability of the host is genetically based, but is affected by a learning process for fine tuning of recognition.     

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.