Bård G. Stokke

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.

Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts?

1. Why are some common and apparently suitable resources avoided by potential users? This interesting ecological and evolutionary conundrum is vividly illustrated by obligate brood parasites. Parasitic birds lay their eggs into nests of a wide range of host species, including many rare ones, but do not parasitize some commonly co-occurring potential hosts. 2. Attempts to explain the absence of parasitism in common potential hosts are limited and typically focused on single-factor explanations while ignoring other potential factors. We tested why thrushes Turdus spp. are extremely rarely parasitized by common cuckoos Cuculus canorus despite breeding commonly in sympatry and building the most conspicuous nests among forest-breeding passerines. 3. No single examined factor explained cuckoo avoidance of thrushes. Life-history traits of all six European thrush species and the 10 most frequently used cuckoo hosts in Europe were similar except body/egg size, nest design and nestling diet. 4. Experiments (n = 1211) in several populations across Europe showed that host defences at egg-laying and incubation stages did not account for the lack of cuckoo parasitism in thrushes. However, cross-fostering experiments disclosed that various factors during the nestling period prevent cuckoos from successfully parasitizing thrushes. Specifically, in some thrush species, the nest cup design forced cuckoo chicks to compete with host chicks with fatal consequences for the parasite. Other species were reluctant to care even for lone cuckoo chicks. 5. Importantly, in an apparently phylogenetically homogenous group of hosts, there were interspecific differences in factors responsible for the absence of cuckoo parasitism. 6. This study highlights the importance of considering multiple potential factors and their interactions for understanding absence of parasitism in potential hosts of parasitic birds. In the present study, comparative and experimental procedures are integrated, which represent a novel approach that should prove useful for the understanding of interspecific ecological relationships in general.

OBLIGATE BROOD PARASITES AS SELECTIVE AGENTS FOR EVOLUTION OF EGG APPEARANCE IN PASSERINE BIRDS

Abstract 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.

Coevolution in action: disruptive selection on egg colour in an avian brood parasite and its host.

Background Trait polymorphism can evolve as a consequence of frequency-dependent selection. Coevolutionary interactions between hosts and parasites may lead to selection on both to evolve extreme phenotypes deviating from the norm, through disruptive selection. Methodology/Principal finding Here, we show through detailed field studies and experimental procedures that the ashy-throated parrotbill (Paradoxornis alphonsianus) and its avian brood parasite, the common cuckoo (Cuculus canorus), have both evolved egg polymorphism manifested in discrete immaculate white, pale blue, and blue egg phenotypes within a single population. In this host-parasite system the most common egg colours were white and blue, with no significant difference in parasitism rates between hosts laying eggs of either colour. Furthermore, selection on parasites for countering the evolution of host egg types appears to be strong, since ashy-throated parrotbills have evolved rejection abilities for even partially mimetic eggs. Conclusions/Significance The parrotbill-cuckoo system constitutes a clear outcome of disruptive selection on both host and parasite egg phenotypes driven by coevolution, due to the cost of parasitism in the host and by host defences in the parasite. The present study is to our knowledge the first to report the influence of disruptive selection on evolution of discrete phenotypes in both parasite and host traits in an avian brood parasitism system.

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.

Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host.

Given the high costs of avian obligate brood parasitism, host individuals are selected to reject parasitic eggs they recognize as foreign. We show that rejection may not necessarily follow egg discrimination when selective removal of the parasitic egg is difficult. We studied egg rejection behaviour in a small host of the common cuckoo Cuculus canorus, the eastern olivaceous warbler Hippolais pallida, by experimental parasitism with model and real non-mimetic cuckoo eggs and video recordings of host behaviour. Hosts pecked 87 per cent (20 out of 23) of the model eggs but eventually accepted 43.5 per cent (10 out of 23) of them. A similar pattern was found for real cuckoo eggs, which were all pecked, but as many as 47 per cent (7 out of 15) of them were accepted. To our knowledge, this is the first demonstration of a cuckoo host discriminating against real parasitic eggs but often accepting them. Our results also show that in host species experiencing difficulties in performing puncture ejection, non-mimetic cuckoo eggs may avoid rejection by means of their unusually high structural strength.

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

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

Avian colour perception predicts behavioural responses to experimental brood parasitism in chaffinches.

Hosts of cuckoos have evolved defences allowing them to discriminate and reject parasite eggs. Mechanisms of discrimination are mostly visually mediated, and have been studied using approaches that do not account for what the receiver (i.e. host) actually can discriminate. Here, for the first time we apply a perceptual model of colour discrimination to study behavioural responses to natural variation in parasite egg appearance in chaffinches Fringilla coelebs. Discrimination of parasite eggs gradually increased with increasing differences in chromatic contrasts as perceived by birds between parasite and host eggs. These results confirm that colour differences of the eggs as perceived by birds are important integral parts of a matching signal used by chaffinch hosts.

The enigma of imperfect adaptations in hosts of avian brood parasites

ABSTRACT Coevolutionary dynamics allow revealing ongoing microevolutionary processes and adaptations. Interactions between obligate avian brood parasites and their hosts are suitable systems for the study of coevolution. This fascinating subject has interested both scientists and the common man for decades, but there are still many unanswered questions. One of the main puzzles is the apparent imperfect rejection behaviour against parasite eggs among hosts of brood parasites leading to a situation where many hosts experience severe costs of parasitism, which dramatically reduce their fitness. In order to lower these costs, hosts are expected to evolve counter-adaptations against parasitism. However, many host species show no rejection or only intermediate rejection rates against non-mimetic parasite eggs. In this review we consider several hypotheses set out to explain this phenomenon, and then we link these hypotheses with a consideration of various sources that can influence decision-making when hosts are faced with the possibility that a parasite egg is present in their nest.

Genetic differentiation among sympatric cuckoo host races: males matter

Generalist parasites regularly evolve host-specific races that each specialize on one particular host species. Many host-specific races originate from geographically structured populations where local adaptations to different host species drive the differentiation of distinct races. However, in sympatric populations where several host races coexist, gene flow could potentially disrupt such host-specific adaptations. Here, we analyse genetic differentiation among three sympatrically breeding host races of the brood-parasitic common cuckoo, Cuculus canorus. In this species, host-specific adaptations are assumed to be controlled by females only, possibly via the female-specific W-chromosome, thereby avoiding that gene flow via males disrupts local adaptations. Although males were more likely to have offspring in two different host species (43% versus 7%), they did not have significantly more descendants being raised outside their putative foster species than females (9% versus 2%). We found significant genetic differentiation for both biparentally inherited microsatellite DNA markers and maternally inherited mitochondrial DNA markers. To our knowledge, this is the first study that finds significant genetic differentiation in biparentally inherited markers among cuckoo host-specific races. Our results imply that males also may contribute to the evolution and maintenance of the different races, and hence that the genes responsible for egg phenotype may be found on autosomal chromosomes rather than the female-specific W-chromosome as previously assumed.