Evolution and genetic architecture of sex-limited polymorphism in cuckoos.

Sex-limited polymorphism has evolved in many species including our own. Yet, we lack a detailed understanding of the underlying genetic variation and evolutionary processes at work. The brood parasitic common cuckoo (Cuculus canorus) is a prime example of female-limited color polymorphism, where adult males are monochromatic gray and females exhibit either gray or rufous plumage. This polymorphism has been hypothesized to be governed by negative frequency-dependent selection whereby the rarer female morph is protected against harassment by males or from mobbing by parasitized host species. Here, we show that female plumage dichromatism maps to the female-restricted genome. We further demonstrate that, consistent with balancing selection, ancestry of the rufous phenotype is shared with the likewise female dichromatic sister species, the oriental cuckoo (Cuculus optatus). This study shows that sex-specific polymorphism in trait variation can be resolved by genetic variation residing on a sex-limited chromosome and be maintained across species boundaries.

Nest sanitation as an effective defence against brood parasitism.

Egg rejection is a crucial defence strategy against brood parasitism that requires the host to correctly recognise the foreign egg. Rejection behaviour has, thus, evolved in many hosts, facilitated by the visual differences between the parasitic and host eggs, and driving hosts to rely on colour and pattern cues. On the other hand, the need to recognise non-egg-shaped objects to carry out nest sanitation led birds to evolve the ability to discriminate and eject objects using mainly shape cues. However, little is known regarding the evolutionary significance of rejection behaviour in general and the cognitive processes underlying it. Here, we investigated the response of the barn swallow (Hirundo rustica) during pre-laying and laying stages to four objects types that differed in shape (eggs vs stars) and colour/pattern (mimetic vs non-mimetic) to investigate (1) what cognitive mechanisms are involved in object discrimination and (2) whether egg rejection is a direct defence against brood parasitism, or simply a product of nest sanitation. We found that swallows ejected stars more often than eggs in both stages, indicating that swallows possess a template for the shape of their eggs. Since the effect of colour/pattern on ejection decisions was minor, we suggest that barn swallows have not evolved a direct defence against brood parasitism but instead, egg ejection might be a product of their well-developed nest sanitation behaviour. Nonetheless, the fact that mimetic eggs were ejected especially in the pre-laying stage shows that nest sanitation could be an effective defence against poorly timed brood parasitism.

Dynamic egg color mimicry.

Evolutionary hypotheses regarding the function of eggshell phenotypes, from solar protection through mimicry, have implicitly assumed that eggshell appearance remains static throughout the laying and incubation periods. However, recent research demonstrates that egg coloration changes over relatively short, biologically relevant timescales. Here, we provide the first evidence that such changes impact brood parasite-host eggshell color mimicry during the incubation stage. First, we use long-term data to establish how rapidly the Acrocephalus arundinaceus Linnaeus (great reed warbler) responded to natural parasitic eggs laid by the Cuculus canorus Linnaeus (common cuckoo). Most hosts rejected parasitic eggs just prior to clutch completion, but the host response period extended well into incubation (~10 days after clutch completion). Using reflectance spectrometry and visual modeling, we demonstrate that eggshell coloration in the great reed warbler and its brood parasite, the common cuckoo, changes rapidly, and the extent of eggshell color mimicry shifts dynamically over the host response period. Specifically, 4 days after being laid, the host should notice achromatic color changes to both cuckoo and warbler eggs, while chromatic color changes would be noticeable after 8 days. Furthermore, we demonstrate that the perceived match between host and cuckoo eggshell color worsened over the incubation period. These findings have important implications for parasite-host coevolution dynamics, because host egg discrimination may be aided by disparate temporal color changes in host and parasite eggs.

Does nest luminosity play a role in recognition of parasitic eggs in domed nests? A case study of the red bishop.

Certain light environments may hinder egg discrimination by hosts of foreign eggs, which could in some circumstances lead to the acceptance of non-mimetic eggs by hosts. We measured light parameters at red bishop (Euplectes orix) nests and used a model of avian visual processing to quantify the detectability of eggs in the light environment in which they are perceived. We found that the overall amount of light was very variable between red bishop nests and always sufficient for colour discrimination. A model of avian visual processing revealed that nest luminosity had no influence on host responses towards eggs which were painted dark brown. Dark eggs do not appear to be cryptic in red bishop nests and can be distinguished with ease, whereas natural red bishop eggs are usually accepted, despite the domed structure of the nest. We found little variation in both chromatic and achromatic contrasts between host and artificial eggs, indicating that there was very little variation in the light quality inside nests. We suggest that nest luminosity is likely to play a role in egg recognition in situations when light reaches threshold values for colour discrimination, i.e. in scotopic as opposed to photopic vision. Rejection rates for dark eggs were higher than for bright (conspecific) foreign eggs. More investigation of domed nest-building species is required, as this type of nest appears to have a highly variable light environment, dependent on both nest structure and habitat.

Brood parasites lay eggs matching the appearance of host clutches.

Interspecific brood parasitism represents a prime example of the coevolutionary arms race where each party has evolved strategies in response to the other. Here, we investigated whether common cuckoos (Cuculus canorus) actively select nests within a host population to match the egg appearance of a particular host clutch. To achieve this goal, we quantified the degree of egg matching using the avian vision modelling approach. Randomization tests revealed that cuckoo eggs in naturally parasitized nests showed lower chromatic contrast to host eggs than those assigned randomly to other nests with egg-laying date similar to naturally parasitized clutches. Moreover, egg matching in terms of chromaticity was better in naturally parasitized nests than it would be in the nests of the nearest active non-parasitized neighbour. However, there was no indication of matching in achromatic spectral characteristics whatsoever. Thus, our results clearly indicate that cuckoos select certain host nests to increase matching of their own eggs with host clutches, but only in chromatic characteristics. Our results suggest that the ability of cuckoos to actively choose host nests based on the eggshell appearance imposes a strong selection pressure on host egg recognition.