Johan Reinert Vikan

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.

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.

Evolution of defences against cuckoo (Cuculus canorus) parasitism in bramblings (Fringilla montifringilla): 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.

Outcomes of Brood Parasite–Host Interactions Mediated by Egg Matching: Common Cuckoos Cuculus canorus versus Fringilla Finches

Background Antagonistic species often interact via matching of phenotypes, and interactions between brood parasitic common cuckoos (Cuculus canorus) and their hosts constitute classic examples. The outcome of a parasitic event is often determined by the match between host and cuckoo eggs, giving rise to potentially strong associations between fitness and egg phenotype. Yet, empirical efforts aiming to document and understand the resulting evolutionary outcomes are in short supply. Methods/Principal Findings We used avian color space models to analyze patterns of egg color variation within and between the cuckoo and two closely related hosts, the nomadic brambling (Fringilla montifringilla) and the site fidelic chaffinch (F. coelebs). We found that there is pronounced opportunity for disruptive selection on brambling egg coloration. The corresponding cuckoo host race has evolved egg colors that maximize fitness in both sympatric and allopatric brambling populations. By contrast, the chaffinch has a more bimodal egg color distribution consistent with the evolutionary direction predicted for the brambling. Whereas the brambling and its cuckoo host race show little geographical variation in their egg color distributions, the chaffinchs distribution becomes increasingly dissimilar to the bramblings distribution towards the core area of the brambling cuckoo host race. Conclusion High rates of brambling gene flow is likely to cool down coevolutionary hot spots by cancelling out the selection imposed by a patchily distributed cuckoo host race, thereby promoting a matching equilibrium. By contrast, the site fidelic chaffinch is more likely to respond to selection from adapting cuckoos, resulting in a markedly more bimodal egg color distribution. The geographic variation in the chaffinchs egg color distribution could reflect a historical gradient in parasitism pressure. Finally, marked cuckoo egg polymorphisms are unlikely to evolve in these systems unless the hosts evolve even more exquisite egg recognition capabilities than currently possessed.

Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts

In avian brood parasitism, egg phenotype plays a key role for both host and parasite reproduction. Several parrotbill species of the genus Paradoxornis are parasitized by the common cuckoo Cuculus canorus, and clear polymorphism in egg phenotype is observed. In this article, we develop a population genetics model in order to identify the key parameters that control the maintenance of egg polymorphism. The model analyses show that egg polymorphism can be maintained either statically as an equilibrium or dynamically with frequency oscillations depending on the sensitivity of the host against unlike eggs and how the parasite targets host nests with specific egg phenotypes. On the basis of the model, we discuss egg polymorphism observed in parrotbills and other host species parasitized by the cuckoo. We suggest the possibility that frequencies of egg phenotypes oscillate and we appeal for monitoring of cuckoo–host interactions over a large spatiotemporal scale.

Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions

Although parasites and their hosts often coexist in a set of environmentally differentiated populations connected by gene flow, few empirical studies have considered a role of environmental variation in shaping correlations between traits of hosts and parasites. Here, we studied for the first time the association between the frequency of adaptive parasitic common cuckoo Cuculus canorus phenotypes in terms of egg matching and level of defences exhibited by its reed warbler Acrocephalus scirpaceus hosts across seven geographically distant populations in Europe. We also explored the influence of spring climatic conditions experienced by cuckoos and hosts on cuckoo–host egg matching. We found that between-population differences in host defences against cuckoos (i.e. rejection rate) covaried with between-population differences in degree of matching. Between-population differences in host egg phenotype were associated with between-population differences in parasitism rate and spring climatic conditions, but not with host level of defences. Between-population differences in cuckoo egg phenotype covaried with between-population differences in host defences and spring climatic conditions. However, differences in host defences still explained differences in mimicry once differences in climatic conditions were controlled, suggesting that selection exerted by host defences must be strong relative to selection imposed by climatic factors on egg phenotypes.

The common cuckoo Cuculus canorus is not locally adapted to its reed warbler Acrocephalus scirpaceus host

The obligate avian brood parasitic common cuckoo Cuculus canorus comprises different strains of females that specialize on particular host species by laying eggs of a constant type that often mimics those of the host. Whether cuckoos are locally adapted for mimicking populations of the hosts on which they are specialized has never been investigated. In this study, we first explored the possibility of local adaptation in cuckoo egg mimicry over a geographical mosaic of selection exerted by one of its main European hosts, the reed warbler Acrocephalus scirpaceus. Secondly, we investigated whether cuckoos inhabiting reed warbler populations with a broad number of alternative suitable hosts at hand were less locally adapted. Cuckoo eggs showed different degrees of mimicry to different reed warbler populations. However, cuckoo eggs did not match the egg phenotypes of their local host population better than eggs of other host populations, indicating that cuckoos were not locally adapted for mimicry on reed warblers. Interestingly, cuckoos exploiting reed warblers in populations with a relatively larger number of co‐occurring cuckoo gentes showed lower than average levels of local adaptation in egg volume. Our results suggest that cuckoo local adaptation might be prevented when different cuckoo populations exploit more or fewer different host species, with gene flow or frequent host switches breaking down local adaptation where many host races co‐occur.

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.