Parentage and host preference in the common cuckoo Cuculus canorus

Microsatellite DNA markers were used to investigate parentage relationships in a population of common cuckoo Cuculus canorus. Thirty adults and 55 nestlings were genotyped at six loci from blood samples collected over a four‐year period. To test whether each cuckoo female specialises in parasitising one single host species (Host Preference Hypothesis), the maternal relationships were used to record each female's host choice. The results supported the Host Preference Hypothesis since no female (N=3) was recorded to have parasitised more than one of four congeneric host species breeding in the area. In contrast, the males (N=4) did not show such specialisation since two of them sired offspring reared by different host species.     

Parentage and host preference in the common cuckoo Cuculus canorus

Microsatellite DNA markers were used to investigate parentage relationships in a population of common cuckoo Cuculus canorus . Thirty adults and 55 nestlings were genotyped at six loci from blood samples collected over a four-year period. To test whether each cuckoo female specialises in parasitising one single host species (Host Preference Hypothesis), the maternal relationships were used to record each female's host choice. The results supported the Host Preference Hypothesis since no female (N=3) was recorded to have parasitised more than one of four congeneric host species breeding in the area. In contrast, the males (N=4) did not show such specialisation since two of them sired offspring reared by different host species.     

Adaptations in the common cuckoo (Cuculus canorus) to host eggs in a multiple-hosts system of brood parasitism

The common cuckoo Cuculus canorus parasitism greatly reduces the reproductive success of its hosts and imposes strong selection pressure for hosts to evolve defences against parasitism, such as the ability to recognize and reject dissimilar parasitic eggs, which, in turn, selects for better egg mimicry by the cuckoo. In the co-evolutionary interaction, however, it remains unknown how the cuckoo successfully expanded its range of host usage and how they developed egg mimicry. Most previous studies were conducted in areas where a very few number of host species (i.e. one or two at most) are sympatric with the cuckoo. Several host species, however, breed sympatric with the cuckoo and have been parasitized in the study site in Nagano, central Japan. Such a multiple-hosts system will provide valuable insights for understanding the cuckoo–hosts interactions in the past. In the present study, we report quantitative profiles of eggs based on spectrometer reflectance for four major host species and the corresponding cuckoo gentes. The hosts include the oriental reed warbler ( Acrocephalus orientalis ), bull-headed shrike ( Lanius bucephalus ), azure-winged magpie ( Cyanopica cyana ), and black-faced bunting ( Emberiza spodocephala ). We show that (1) egg morphs of each host and corresponding cuckoo gens can be categorized by two chromatic components of reflectance spectra and (2) there is a significant difference in a particular chroma component between hosts and the cuckoo. We suggest that the cuckoo parasitism in central Japan originated from parasitism on the black-faced bunting.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 291–300.     

A comparative study of host selection in the European cuckoo Cuculus canorus

Certain kinds of hosts are commonly regarded as being more suitable than other for rearing European cuckoos (Cuculus canorus) – insectivores that lay small eggs and have open, shallow nests – although empirical tests of cuckoo host selection are lacking. We analysed host use by the European cuckoo in 72 British passerines that are potential hosts and for which there was information available on life-history variables and variables related to cuckoo-host coevolution, such as rate of parasitism, rejection rate of non-mimetic model eggs and degree of cuckoo-egg mimicry of host eggs. The relative population size of the host species affected parasitism rate most strongly, followed by relatively short duration of the nestling period, and the kind of nest, with cuckoos selecting open-nesting hosts. However, the effect of the nestling period could be related to host body size and the kind of nest used, because hole-nesting species normally have longer nestling periods than open-nesters. We re-analysed the data excluding hole nesters and corvid species (species with larger body mass), but the results remained identical. The European cuckoo may benefit from selecting hosts with short nestling periods because such hosts provide food for their nestlings at a very high rate. When only those species known as cuckoo hosts were analysed, the variable that best accounted for the parasitism rate was duration of the breeding season. Therefore, availability of potential hosts in both time and space is important for cuckoos in selecting hosts. Received: 16 July 1998 / Accepted: 27 October 1998     

Sex allocation in relation to host races in the brood-parasitic common cuckoo (Cuculus canorus)

Sex allocation theory and empirical evidence both suggest that natural selection should favour maternal control of offspring sex ratio in relation to their ability to invest in the offspring. Generalist parasites constitute a particularly interesting group to test this theory as different females commonly utilize different host species showing large variation in provisioning ability. The common cuckoo (Cuculus canorus) is a generalist brood parasite that lays its eggs in the nest of many different passerine birds, but each female tends to specialize on one particular host species giving rise to highly specialized host races. The different host species show large variation in their ability to invest in the parasitic offspring, presenting an opportunity for female cuckoos to bias offspring sex ratio in relation to host species quality. Here, we investigate host-race specific sex allocation controlling for maternal identity in the common cuckoo. We found no evidence of any significant relationship between host race and sex ratio in one sympatric population harbouring three different host races, or in a total of five geographically separated populations. There was also no significant association between host quality, as determined by species-specific female host body mass, and cuckoo sex ratio. Finally, we found no significant relationship between individual cuckoo maternal quality, as determined by her egg volume, and sex ratio within each host race. We conclude that the generalist brood-parasitic common cuckoo show no significant sex-ratio bias in relation to host race and discuss this finding in light of gene flow and host adaptations.     

中国大杜鹃的鸣声

一直以来认为广布欧洲大陆和亚洲大陆的大杜鹃 ,其鸣声在地区之间无差异 ,而分布在亚洲的大杜鹃的鸣声至今未有系统的研究报道。本文以分布在中国北部的大杜鹃指名亚种和新疆亚种的广告鸣叫为主要研究对象 ,将其与在四川和云南省分布的大杜鹃华西亚种以及分布在朝鲜、日本、俄罗斯和英格兰的大杜鹃指名亚种的广告鸣叫进行了初步比较。在中国分布的大杜鹃有五种鸣叫类型。中国所有采集地大杜鹃的广告鸣叫都由两个音节组成 ,并且与英国分布种群的广告鸣叫很相似。各地大杜鹃的领域鸣唱呈现出个体质的高度保守性和数量性状的明显差异     

Eviction behaviour of the common cuckoo Cuculus canorus chicks

We studied the eviction behaviour of common cuckoo Cuculus canorus chicks by video recording at nests of great reed warblers Acrocephalus arundinaceus and reed warblers Acrocephalus scirpaceus . There were no significant differences in hatching mass and age at first eviction between cuckoos reared by either host. However, mass at eviction had a significant effect on the timing of first eviction event. No significant difference in time required to evict was found between serial intranest eviction events for cuckoos raised by either host. However, "great reed warbler" cuckoos evicted significantly quicker than "reed warbler" cuckoos during particular eviction events. A majority (70%) of "reed warbler" cuckoos evicted during the day, while most "great reed warbler" cuckoos evicted nocturnally (63%). We did not find any effect of the temperature inside or outside the nest on eviction behaviour. Both "great reed warbler" and "reed warbler" cuckoos evicted regardless the fact whether a parent was absent or present at the nest. Interestingly, individual cuckoos were consistent in their eviction behaviour relative to host presence or absence; particular cuckoo chick evicted only when the parents were present or absent from the nest.     

Rejection of cuckoo (Cuculus canorus) eggs by meadow pipits (Anthus pratensis)

Meadow pipits (Anthus pratensis) normally accept mimetic cuckoo(Cuculus canorus) eggs laid in their nests. In field experimentsin which a mimetic or a nonmimetic model cuckoo egg was placedin meadow pipit nests, those hosts that were simultaneouslypresented with a cuckoo dummy mounted beside the nest showeda significantly higher ability to recognize and reject (normallyby desertion) the parasite's egg than those that were not presentedwith the dummy. In the present study we sought to answer thequestion of why meadow pipits do not always (i.e., even whenno cuckoo was visible) reject cuckoo eggs. The results fromthe field experiments provide support for a theory that two"brood parasite" stimuli (a cuckoo egg in the nest and a cuckoonear the nest) are necessary to induce the meadow pipits toreject cuckoo eggs. When the threshold for rejection had beenreached, the hosts reacted in a relatively short time afterthey were faced with the parasite stimuli. The results of theseexperiments also showed that a significantly higher rate ofrejection occurred earlier rather than later in the incubationperiod. A possible explanation for the higher rate of acceptanceof model cuckoo eggs among meadow pipits in Norway comparedto those in Britain is discussed.     

Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change

Parasites require synchrony with their hosts so if host timing changes with climate change, some parasites may decline and eventually go extinct. Residents and short-distance migrant hosts of the brood parasitic common cuckoo, Cuculus canorus, have advanced their phenology in response to climate change more than long-distance migrants, including the cuckoo itself. Because different parts of Europe show different degrees of climate change, we predicted that use of residents or short-distance migrants as hosts should have declined in areas with greater increase in spring temperature. Comparing relative frequency of parasitism of the two host categories in 23 European countries before and after 1990, when spring temperatures in many areas had started to increase, we found that relative parasitism of residents and short-distance migrants decreased. This change in host use was positively related to increase in spring temperature, consistent with the prediction that relative change in phenology for different migrant classes drives host-use patterns. These findings are consistent with the hypothesis that climate change affects the relative abundance of different host races of the common cuckoo.     

How is host egg mimicry maintained in the cuckoo (Cuculus canorus)?

To investigate the evolutionary mechanism (host specificity vs. random searching) maintaining mimicry between cuckoo egg appearance and that of different European cuckoo Cuculus canorus hosts, we studied the level of mimicry between the appearance of C. canorus eggs and that of their hosts' eggs in different habitats in southern Finland by using ultraviolet-visible reflectance spectrophotometry. In the main habitat used by C. canorus for reproduction, eggs laid in nests of different host species differed in appearance. Host use by C. canorus was not related to the abundance of hosts, and the level of mimicry was not related to host abundance in the habitat. Furthermore, a close match between C. canorus egg appearance and that of host eggs within habitats was detected after removing the potentially confounding effect of host abundance. In the only two suitable host species nesting in trees (namely chaffinch Fringilla coelebs and brambling Fringilla montifringilla ) we detected changes in C. canorus egg appearance that paralleled those of the two host species. Thus our findings suggest the existence of a correlation between the appearance of C. canorus eggs and that of their hosts' eggs within different habitat types, and suggest that mimicry is maintained by strict host preferences by each C. canorus female when laying.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 57–68.     

Rejection of common cuckoo Cuculus canorus eggs in relation to female age in the bluethroat Luscinia svecica

The evolutionary equilibrium hypothesis explains the existence of both acceptors and rejecters of brood parasite eggs within a host population as resulting from a balance between the costs of acceptance and the costs of recognition errors. In such equilibria conditional responses may play an important role. One such response that has been demonstrated in one common cuckoo Cuculus canorus host species is that first year, naive breeders accept parasitic eggs at a higher frequency than older and more experienced birds do. In the present study we tested whether this is the response in the bluethroat Luscinia svecica. We did not find any difference in rejection behaviour between first-year breeders and older birds. This finding is discussed in relation to recognition costs, cuckoo egg mimicry and the bluethroat's present status as a host. We conclude that the results are best explained by the evolutionary lag hypothesis.     

Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function

Some parasite cuckoo species lay eggs that, to the human eye, appear to mimic the appearance of the eggs of their favourite hosts, which hinders discrimination and removal of their eggs by host species. Hitherto, perception of cuckoo-host egg mimicry has been estimated based on human vision or spectrophotometry, which does not account for what the receivers' eye (i.e. hosts) actually discriminates. Using a discrimination model approach that reproduces host retinal functioning, and museum egg collections collected in the south of Finland, where at least six different races of the European cuckoo (Cuculus canorus) coexist, I first assess whether the colour design of cuckoo eggs of different races maximizes matching for two favourite avian hosts, viz. the redstart (Phoenicurus phoenicurus) and the pied wagtail (Motacilla alba). Second, I assess the role of nest luminosity on host perception of mimicry by the same two hosts. Phoenicurus-cuckoo eggs showed a better chromatic matching with the redstart-host eggs than other cuckoo races, and in most cases can not be discriminated. Sylvia-cuckoo eggs, however, showed better achromatic matching with redstart-host eggs than Phoenicurus-cuckoo eggs. Also, Motacilla-cuckoo eggs showed poorer chromatic and achromatic matching with pied wagtail-host eggs than Sylvia-cuckoo eggs. Nest luminosity affected chromatic and achromatic differences between cuckoo and host eggs, although only minimally affected the proportion of cuckoo eggs discriminated by chromatic signals. These results reveal that cuckoo races as assessed by humans do not entirely match with host perception of matching and that achromatic mechanisms could play a main role in the discrimination of cuckoo eggs at low-light levels.     

Unrealistically high costs of rejecting artificial model eggs in cuckoo Cuculus canorus hosts

Most studies that have tested the egg-recognition and egg-rejection ability of European cuckoo Cuculus canorus hosts have used artificial model eggs that are much harder than real Cuckoo eggs. Here we evaluate whether the use of such models overestimates the costs of egg rejection by hosts. We tested 17 potential cuckoo host species in south-eastern Spain with both artificial hard cuckoo-egg models and real eggs taken from a population of house sparrows Passer domesticus breeding in captivity. The puncture resistance of sparrow eggs, measured in the laboratory, was more similar to that of real cuckoo eggs than was the resistance of artificial models, although sparrow eggs were less resistant than real cuckoo eggs. Potential host species with a grasp index greater than 200 mm² did not suffer high rejection costs when rejecting hard models, probably because they are grasp ejectors. However, all species with a smaller grasp index suffered high costs when rejecting hard artificial models. For these species the frequency and magnitude of costs were significantly higher when rejecting artificial hard models than when rejecting real eggs. For some species the breakage of real eggs was quite difficult (they needed 97 to more than 4000 pecks in video-recorded ejections), and sometimes the birds suffered rejection costs. These results show that realistic estimates of the frequency and magnitude of rejection costs for hosts with small bills cannot be obtained by using artificial models, and also that for a variety of medium-sized puncture ejector species the costs when rejecting real eggs may be low.     

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

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

Factors influencing the risk of common cuckoo Cuculus canorus parasitism on marsh warblers Acrocephalus palustris

Using multiple logistic regression analysis, we investigated the influence of nest site characteristics, laying date and nest size in marsh warblers Acrocephalus palustris on the risk of parasitism by common cuckoos Cuculus canorus . Marsh warblers breed in more diverse and dense herbaceous vegetation than other cuckoo hosts investigated in comparable studies. The "perch proximity" hypothesis was supported as parasitized nests were situated closer to trees than non-parasitized ones. Furthermore, demonstrated for the first time in a cuckoo host, tree height was an important predictor of parasitism, with higher trees increasing the parasitism odds ratio. The "nest exposure" hypothesis was also supported since parasitized nests had a shorter stand of vegetation in the close vicinity than non-parasitized nests. However, visibility of the nest from the nearest potential cuckoo perch (cuckoo view) was not selected by the model, probably because most nests were well concealed. Laying date, height of nest above ground and the distance from the nest to the nearest edge of the vegetation were not important predictors of parasitism. Though smaller nests tended to be parasitized more frequently than larger ones, nest size only approached significance, making its importance unclear.     

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.     

Geographic distribution of suitable hosts explains the evolution of specialized gentes in the European cuckoo Cuculus canorus

Background

We recently discovered two composite long terminal repeat (LTR)-retrotransposon-like elements which we named DA (~300 kb) and Xiao (~30 kb), meaning big and small in Chinese respectively. Xiao and DA (three types of DA identified) were found to have been derived from several donor sites and have spread to 30 loci in the human genome, totaling to 5 Mb. Our bioinformatics analyses with the released human, chimp, rhesus macaque, orangutan, and marmoset genomic sequences indicate that DA and Xiao emerged ~25 million years (Myr) ago.

Results

To better understand the evolution of these two complex elements, we investigated various internal junctions of DA and Xiao as well as orthologous genomic sites of the 30 DA/Xiao loci in non-human primates including great apes, lesser apes, Old World monkeys, New World monkeys, and a prosimian. We found that Xiao and type I DA first emerged in the genome between 25 and 18 Myr ago, whereas type II and Type III DAs emerged between 14 and 7 Myr ago. Xiao and DA were most active in great apes, with their amplification peaking during 25-14 and 14-7 Myr ago, respectively. Neither DA nor Xiao seem to have been active in the human and chimp genomes during last 6 Myr.

Conclusion

The study has led to a more accurate age determination of the DA and Xiao elements than our previous bioinformatics analyses, and indicates that the amplification activity of the elements coincided with that of group I HERV-Es during evolution. It has also illustrated an evolutionary path with stepwise structural changes for the elements during past 25 Myr, and in doing so has shed more light on these two intriguing and complex elements that have reshaped our genome.     

Meadow pipit (Anthus pratensis) egg appearance in cuckoo (Cuculus canorus) sympatric and allopatric populations

Host populations tend to show less ability to discriminate against parasites when living in their absence. However, comparison of rejection rates among sympatric and allopatric host populations does not allow determination of whether the greater tolerance in allopatric populations reflects a genetic change or phenotypic plasticity. Here we test the existence of changes in a host's adaptation to brood parasitism in the absence of parasitism by studying intraclutch variation in egg appearance, which is a genetically determined component of host defence favouring discrimination of parasitic eggs. We investigated egg phenotypes of a common host of the European cuckoo, Cuculus canorus , in the presence and in the absence of cuckoos. By using objective spectroradiometry techniques of colour assessment we compared intraclutch variation between populations of meadow pipit, Anthus pratensis , sympatric (England) and allopatric (Iceland and Faeroe Islands) with C. canorus . Allopatric populations of A. pratensis showed greater intraclutch variation in egg appearance in the ultraviolet part of the spectrum than did a population sympatric with C. canorus . Two possible alternative mechanisms explaining these findings are discussed.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 543–549.     

Errors in egg-laying by female Common Cuckoo Cuculus canorus in nests of its common host

Dozens of studies have documented that brood parasites are well adapted to a brood parasitic lifestyle but not all parasitism events are successful. Co-evolution between brood parasites and their hosts is a dynamic process so it is reasonable to expect that a female brood parasite may commit errors during egg deposition by laying her eggs outside the laying period of the host, with consequent impacts on her fitness. Using an extensive dataset from a long-term study, we evaluated egg-laying patterns and errors related to the timing of egg-laying in the Common Cuckoo Cuculus canorus (hereafter ‘Cuckoo’). Specifically, we tested whether the Cuckoo avoids laying before or on the day of host clutch initiation to reduce the risk of rejection of parasitic eggs, whether laying errors will be more frequent in periods with a lack of active host nests, and whether the laying errors will be more frequent in periods with intense Cuckoo parasitism and a consequent lack of suitable host nests. We found that about one-third of Cuckoo eggs were laid on the host clutch initiation day or 1 day before, and the percentage of Cuckoo eggs laid decreased thereafter. Surprisingly, the probability of Cuckoo egg acceptance by the hosts was not affected by the egg-laying stage of the host clutch. Errors in the timing of egg-laying with fatal consequences (i.e. those precluding Cuckoo hatching because of laying in incubated or deserted clutches) were recorded in about 5% of cases. Only laying date of a Cuckoo egg had a significant effect on the probability of errors, which increased during the breeding season. This may be related to the higher number of deserted and incubated host nests at the site at the end of the breeding season. Errors in egg-laying may be attributed to young and inexperienced females but also impaired body condition or intraspecific competition may cause this behaviour. Future studies, which will test these possible explanations, will help to understand better the mechanism of co-evolutionary arms races and differences between host specialist and generalist brood parasites in various host–parasite systems.     

A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species

The common cuckoo has several host-specific races, each with a distinctive egg that tends to match its host's eggs. Here, we show that the host-race specializing on reed warblers also has a host-specific nestling adaptation. In playback experiments, the nestling cuckoos responded specifically to the reed warbler's distinctive 'churr' alarm (given when a predator is near the nest), by reducing begging calls (likely to betray their location) and by displaying their orange-red gape (a preparation for defence). When reed warbler-cuckoos were cross-fostered and raised by two other regular cuckoo hosts (robins or dunnocks), they did not respond to the different alarms of these new foster-parents. Instead, they retained a specific response to reed warbler alarms but, remarkably, increased both calling and gaping. This suggests innate pre-tuning to reed warbler alarms, but with exposure necessary for development of the normal silent gaping response. By contrast, cuckoo chicks of another host-race specializing on redstarts showed no response to either redstart or reed warbler alarms. If host-races are restricted to female cuckoo lineages, then chick-tuning in reed warbler-cuckoos must be under maternal control. Alternatively, some host-races might be cryptic species, not revealed by the neutral genetic markers studied so far.