Light matters: Nest illumination alters egg rejection behavior in a cavity-nesting bird

Inferences about mechanisms at one particular stage of a visual pathway may be made from psychophysical thresholds only if the noise at the stage in question dominates that in the others. Spectral sensitivities, measured under bright conditions, for di-, tri-, and tetrachromatic eyes from a range of animals can be modelled by assuming that thresholds are set by colour opponency mechanisms whose performance is limited by photoreceptor noise, the achromatic signal being disregarded. Noise in the opponency channels themselves is therefore not statistically independent, and it is not possible to infer anything more about the channels from psychophysical thresholds. As well as giving insight into mechanisms of vision, the model predicts the performance of colour vision in animals where physiological and anatomical data on the eye are available, but there are no direct measurements of perceptual thresholds. The model, therefore, is widely applicable to comparative studies of eye design and visual ecology.

One of the most striking outcomes of coevolution between species is egg mimicry by brood parasitic birds, resulting from rejection behavior by discriminating host parents. Yet, how exactly does a host detect a parasitic egg? Brood parasitism and egg rejection behavior provide a model system for exploring the relative importance of different visual cues used in a behavioral task. Although hosts are discriminating, we do not know exactly what cues they use, and to answer this it is crucial to account for the receiver's visual perception. Color, luminance ("perceived lightness") and pattern information have never been simultaneously quantified and experimentally tested through a bird's eye. The cuckoo finch Anomalospiza imberbis and its hosts show spectacular polymorphisms in egg appearance, providing a good opportunity for investigating visual discrimination owing to the large range of patterns and colors involved. Here we combine field experiments in Africa with modeling of avian color vision and pattern discrimination to identify the specific visual cues used by hosts in making rejection decisions. We found that disparity between host and foreign eggs in both color and several aspects of pattern (dispersion, principal marking size, and variability in marking size) were important predictors of rejection, especially color. These cues correspond exactly to the principal differences between host and parasitic eggs, showing that hosts use the most reliable available cues in making rejection decisions, and select for parasitic eggs that are increasingly mimetic in a range of visual attributes.

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.