Fitting different visual models to behavioral patterns of parasitic egg rejection along a natural egg color gradient in a cavity-nesting host species.

Avian brood parasites lay their eggs in other birds' nests, and hosts can mitigate the fitness cost of raising unrelated offspring by rejecting parasitic eggs. A visually-based cognitive mechanism often thought to be used by hosts to discriminate the foreign egg is to compare it against the hosts' own eggshell by size, shape, maculation, and/or ground coloration (i.e., absolute chromatic contrast). However, hosts may instead discriminate eggs based on their colors along a scale of natural avian eggshell coloration (i.e., directional chromatic contrast). In support of this latter visual process, recent research has found that directional chromatic contrasts can explain some host species' rejection behavior better than absolute chromatic or achromatic contrasts. Here, for the first time, we conducted an experiment in a cavity-nesting host species to test the predictions of these different visual mechanisms. We experimentally parasitized nests of the Common Redstart Phoenicurus phoenicurus, a regular host of a mimetic-egg laying Common Cuckoo Cuculus canorus host-race, using painted, immaculate 3D-printed model eggs in two geographically distant areas (Finland and Czech Republic). We found that directional chromatic contrasts better explained rejection behaviors in both parasitized (Finland) and non-parasitized (Czech Republic) host populations, as hosts rejected eggs that were noticeably browner, but not eggs that were noticeably bluer, than redstart eggs. These results support the paradigm of a single rejection threshold predicted by the directional chromatic contrast model and contribute to a growing generality of these patterns across diverse avian host-brood parasite systems.

Multiple parasitism reduces egg rejection in the host (Acrocephalus arundinaceus) of a mimetic avian brood parasite (Cuculus canorus).

A host that has been targeted by an avian brood parasite can recover most of its potential fitness loss by ejecting the foreign egg(s) from its nest. The propensity for some hosts to engage in egg rejection behavior has put selective pressure on their parasites to evolve mimetic eggshells resembling the host's own shell colors and maculation. In turn, hosts have counterevolved increasingly more sophisticated detection methods such as narrowing visual egg acceptance thresholds or using social cues to recognize parasitism. However, multiple cognitive mechanisms acting simultaneously could theoretically interfere with one another and ultimately decrease egg rejection accuracy, especially if these heuristics yield differing targets for rejection. By painting hosts own eggs, we studied a host species of the common cuckoo Cuculus canorus, the great reed warbler Acrocephalus arundinaceus, and tested its responses to the presence of "foreign" eggs of varying quantity, colors, and uniformity. Using reflectance spectra of egg background coloration and avian perceptual modeling, we then estimated the sensory thresholds triggering egg rejection by this host for each treatment. As previously reported, rejection rates were positively related to the perceptual distance between own and foreign eggs in the nests in all treatments. However, rejection thresholds were more permissive (error prone) both with greater proportions of foreign eggs per clutch and/or when the suite of foreign eggs was perceptually more variable within the nest. These results suggest that parasites, through multiple parasitism, can partially overcome the evolution of hosts' recognition of mimetic parasite eggs. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Shared neural substrates for song discrimination in parental and parasitic songbirds.

In many social animals, early exposure to conspecific stimuli is critical for the development of accurate species recognition. Obligate brood parasitic songbirds, however, forego parental care and young are raised by heterospecific hosts in the absence of conspecific stimuli. Having evolved from non-parasitic, parental ancestors, how brood parasites recognize their own species remains unclear. In parental songbirds (e.g. zebra finch Taeniopygia guttata), the primary and secondary auditory forebrain areas are known to be critical in the differential processing of conspecific vs. heterospecific songs. Here we demonstrate that the same auditory brain regions underlie song discrimination in adult brood parasitic pin-tailed whydahs (Vidua macroura), a close relative of the zebra finch lineage. Similar to zebra finches, whydahs showed stronger behavioral responses during conspecific vs. heterospecific song and tone pips as well as increased neural responses within the auditory forebrain, as measured by both functional magnetic resonance imaging (fMRI) and immediate early gene (IEG) expression. Given parallel behavioral and neuroanatomical patterns of song discrimination, our results suggest that the evolutionary transition to brood parasitism from parental songbirds likely involved an "evolutionary tinkering" of existing proximate mechanisms, rather than the wholesale reworking of the neural substrates of species recognition.