Golo Maurer

Visual mimicry of host nestlings by cuckoos

Coevolution between antagonistic species has produced instances of exquisite mimicry. Among brood-parasitic cuckoos, host defences have driven the evolution of mimetic eggs, but the evolutionary arms race was believed to be constrained from progressing to the chick stage, with cuckoo nestlings generally looking unlike host young. However, recent studies on bronze-cuckoos have confounded theoretical expectations by demonstrating cuckoo nestling rejection by hosts. Coevolutionary theory predicts reciprocal selection for visual mimicry of host young by cuckoos, although this has not been demonstrated previously. Here we show that, in the eyes of hosts, nestlings of three bronze-cuckoo species are striking visual mimics of the young of their morphologically diverse hosts, providing the first evidence that coevolution can select for visual mimicry of hosts in cuckoo chicks. Bronze-cuckoos resemble their own hosts more closely than other host species, but the accuracy of mimicry varies according to the diversity of hosts they exploit.

Socially Acquired Host-Specific Mimicry and the Evolution of Host Races in Horsfield'S Bronze-Cuckoo Chalcites Basalis

Abstract Coevolution between parasites and their hosts typically leads to increasing specialization on host species by the parasite. Where multiple hosts are parasitized, specialization on each host can result in genetic divergence within the parasite population to create host races, and, ultimately, new species. We investigate how host-specific traits arise in Horsfields bronze-cuckoo Chalcites basalis nestlings. Newly hatched cuckoos evict host young from the nest, yet in the absence of a model they accurately mimic the different begging calls of a primary host (superb fairy-wren, Malurus cyaneus) and a secondary host (buff-rumped thornbill, Acanthiza reguloides). Using cross-fostering experiments, we show that begging calls are modified after parasitism, through experience. Further, we demonstrate the mechanism by which mimetic calls are acquired. All cuckoo nestlings initially produced the call of their primary host. When cross-fostered as eggs to a secondary host, calls increased in variability and were rapidly modified to resemble those of the secondary host through shaping by host parents. We suggest that plasticity in the development of host-specific traits after parasitism is likely to reduce selection for host race formation.

Are dark cuckoo eggs cryptic in host nests

The coevolutionary arms race between cuckoos and their hosts has famously yielded cuckoo eggs that evade host recognition and rejection by mimicking the appearance of the hosts own clutch. But not all coevolutionary interactions between cuckoos and hosts have followed the same pathway. Several host species do not show egg rejection even when the cuckoos egg looks entirely unlike their own. For example, hosts of some Australian bronze-cuckoos, Chalcites spp., routinely accept olive-brown cuckoo eggs that look very different from the speckled white eggs of their own clutch. Here we investigate the hypothesis that these cuckoo eggs are cryptic, which might explain why hosts do not remove them from their clutch. First, we use a phylogenetic analysis to show that dark bronze-cuckoo eggs are not ancestral, but instead have evolved in a group that parasitizes hosts with dark nests exclusively. Second, we show that dark bronze-cuckoo eggs are laid by two species that parasitize hosts with relatively dark nests, whereas a congeneric bronze-cuckoo species parasitizing host nests with greater ambient light levels lays a mimetic egg. Finally, we use a model of avian visual processing to show that the dark eggs of Goulds bronze-cuckoo C. russatus are cryptic in dark host nests. Our results support the hypothesis that some bronze-cuckoo species and their hosts have pursued an alternative coevolutionary trajectory, which has resulted in the evolution of cryptic, rather than mimetic, cuckoo eggs.

Variability in Avian Eggshell Colour: A Comparative Study of Museum Eggshells

Background The exceptional diversity of coloration found in avian eggshells has long fascinated biologists and inspired a broad range of adaptive hypotheses to explain its evolution. Three main impediments to understanding the variability of eggshell appearance are: (1) the reliable quantification of the variation in eggshell colours; (2) its perception by birds themselves, and (3) its relation to avian phylogeny. Here we use an extensive museum collection to address these problems directly, and to test how diversity in eggshell coloration is distributed among different phylogenetic levels of the class Aves. Methodology and Results Spectrophotometric data on eggshell coloration were collected from a taxonomically representative sample of 251 bird species to determine the change in reflectance across different wavelengths and the taxonomic level where the variation resides. As many hypotheses for the evolution of eggshell coloration assume that egg colours provide a communication signal for an avian receiver, we also modelled reflectance spectra of shell coloration for the avian visual system. We found that a majority of species have eggs with similar background colour (long wavelengths) but that striking differences are just as likely to occur between congeners as between members of different families. The region of greatest variability in eggshell colour among closely related species coincided with the medium-wavelength sensitive region around 500 nm. Conclusions The majority of bird species share similar background eggshell colours, while the greatest variability among species aligns with differences along a red-brown to blue axis that most likely corresponds with variation in the presence and concentration of two tetrapyrrole pigments responsible for eggshell coloration. Additionally, our results confirm previous findings of temporal changes in museum collections, and this will be of particular concern for studies testing intraspecific hypotheses relating temporal patterns to adaptation of eggshell colour. We suggest that future studies investigating the phylogenetic association between the composition and concentration of eggshell pigments, and between the evolutionary drivers and functional impacts of eggshell colour variability will be most rewarding.

Impact of time since collection on avian eggshell color: a comparison of museum and fresh egg specimens

Studies of avian eggshell coloration have been a long-standing research focus in behavioral evolutionary ecology. Museum collections have provided a widely used resource because they allow efficient sampling across broad temporal, geographical, and taxonomic ranges, even for species that are rare and for which sampling in the wild is ethically or practically unwarranted. We used reflectance spectrophotometry across the avian visual spectrum to compare eggshell color of specimens of the song thrush (Turdus philomelos) in two museums (Natural History Museum, UK and Auckland Museum, New Zealand) with each other and with eggshells collected fresh in New Zealand. These data enabled us to test the effects of source and storage in different museums, as well as time since collection, across four metrics of eggshell coloration: blue-green and ultraviolet chroma, overall brightness, and the spectral coefficient of variation. Variation within an egg, within a clutch, and among clutches, was similar between the two museum datasets but different from those of fresh eggs. We found significant differences in all four metrics between the collections, and that fresh eggshells reflected stronger in the blue-green wavelength than in museum eggs. This difference is most likely due to different preservation techniques and storage histories. Furthermore, an effect of time since collection was only apparent in the blue-green chroma and was higher in more recent museum eggshell samples. Our results support the use of historic museum samples in intraspecific studies of shell coloration providing that efforts are made to compare specimens, which were collected during similar periods.

First light for avian embryos: eggshell thickness and pigmentation mediate variation in development and UV exposure in wild bird eggs

Summary 1. The avian embryo’s development is influenced by both the amount and the wavelength of the light that passes through the eggshell. Commercial poultry breeders use light of specific wavelengths to accelerate embryonic growth, yet the effects of the variably patterned eggshells of wild bird species on light transmission and embryonic development remain largely unexplored. 2. Here, we provide the first comparative phylogenetic analysis of light transmission, through a diverse range of bird eggshells (74 British breeding species), in relation to the eggshell’s thickness, permeability, pigment concentration and surface reflectance spectrum (colour). 3. The percentage of light transmitted through the eggshell was measured in the spectral range 250–700 nm. Our quantitative analyses confirm anecdotal reports that eggshells filter the light of the externally coloured shell. Specifically, we detected a positive relationship between surface eggshell reflectance (‘brightness’) and the percentage of light transmitted through the eggshell, and this relationship was strongest at wavelengths in the human-visible blue-green region of the spectra (c. 435 nm). 4. We show that less light passes through thicker eggshells with greater total pigment concentrations. By contrast, permeability (measured as water vapour conductance) did not covary significantly with light transmission. Eggs of closed-nesting species let more light pass through, compared with open nesters. 5. We postulate that greater light transmission is required to assist embryonic development under low light exposure. Importantly, this result provides an ecological explanation for the repeated evolution of immaculate, white- or pale-coloured eggshells in species nesting in enclosed spaces. 6. Finally, we detected correlative support for the solar radiation hypothesis, in that eggshells of bird species with a longer incubation period let significantly less of the potentially harmful, ultraviolet (UV) light pass through the eggshell. In summary, we demonstrate suites of avian eggshell properties, including eggshell structure and pigmentation, which are consistent with an evolutionary pressure to both enhance and protect embryonic development.

Nesting behaviour influences species-specific gas exchange across avian eggshells.

Carefully controlled gas exchange across the eggshell is essential for the development of the avian embryo. Water vapour conductance (GH2O) across the shell, typically measured as mass loss during incubation, has been demonstrated to optimally ensure the healthy development of the embryo while avoiding desiccation. Accordingly, eggs exposed to sub-optimal gas exchange have reduced hatching success. We tested the association between eggshell GH2O and putative life-history correlates of adult birds, ecological nest parameters and physical characteristics of the egg itself to investigate how variation in GH2O has evolved to maintain optimal water loss across a diverse set of nest environments. We measured gas exchange through eggshell fragments in 151 British breeding bird species and fitted phylogenetically controlled, general linear models to test the relationship between GH2O and potential predictor parameters of each species. Of our 17 life-history traits, only two were retained in the final model: wet-incubating parent and nest type. Eggs of species where the parent habitually returned to the nest with wet plumage had significantly higher GH2O than those of parents that returned to the nest with dry plumage. Eggs of species nesting in ground burrows, cliffs and arboreal cups had significantly higher GH2O than those of species nesting on the ground in open nests or cups, in tree cavities and in shallow arboreal nests. Phylogenetic signal (measured as Pagels λ) was intermediate in magnitude, suggesting that differences observed in the GH2O are dependent upon a combination of shared ancestry and species-specific life history and ecological traits. Although these data are correlational by nature, they are consistent with the hypothesis that parents constrained to return to the nest with wet plumage will increase the humidity of the nest environment, and the eggs of these species have evolved a higher GH2O to overcome this constraint and still achieve optimal water loss during incubation. We also suggest that eggs laid in cup nests and burrows may require a higher GH2O to overcome the increased humidity as a result from the confined nest microclimate lacking air movements through the nest. Taken together, these comparative data imply that species-specific levels of gas exchange across avian eggshells are variable and evolve in response to ecological and physical variation resulting from parental and nesting behaviours.

Conspicuous eggs and colourful hypotheses: testing the role of multiple influences on avian eggshell appearance

The diversity of eggshell colours and patterning across different birds is a fascinating example of the extended avian phenotype. The avian eggs background colours range from light green/yellow to brilliant blue and intense maroon, and with the scrawling patterns comparable to the assortment of eggs found in an Easter Bunnys basket. Here we briefly introduce the diversity of eggshell appearance, its perplexingly narrow chemical basis, and clarify how the a priori assessment of assumptions and potential hypotheses can shape new eggshell research. In addition, we highlight some of the recent hypotheses developed outside the visual paradigm that has dictated the most influential hypotheses of eggshell appearance to date. Finally, we indicate priority areas for future comprehensive research on eggshells based on adaptations to ongoing changes in environmental conditions.

Eggshell Permeability: A Standard Technique for Determining Interspecific Rates of Water Vapor Conductance

Typically, eggshell water vapor conductance is measured on whole eggs, freshly collected at the commencement of a study. At times, however, it may not be possible to obtain whole fresh eggs but rather egg fragments or previously blown eggs. Here we evaluate and describe in detail a technique for modern laboratory analysis of eggshell conductance that uses fragments from fresh and museum eggs to determine eggshell water vapor conductance. We used fresh unincubated eggs of domesticated chickens (Gallus gallus domesticus), ducks (Anas platyrhynchos domesticus), and guinea fowl (Numida meleagris) to investigate the reliability, validity, and repeatability of the technique. To assess the suitability of museum samples, museum and freshly collected black-headed gull eggs (Larus ridibundus) were used. Fragments were cut out of the eggshell from the blunt end (B), equator (E), and pointy end (P). Eggshell fragments were glued to the top of a 0.25-mL micro test tube (Eppendorf) filled with 200 μL of distilled water and placed in a desiccator at 25°C. Eppendorfs were weighed three times at 24-h intervals, and mass loss was assumed to be a result of water evaporation. We report the following results: (1) mass loss between weighing sessions was highly repeatable and consistent in all species; (2) the majority of intraspecific variability in eggshell water vapor conductance between different eggs of the same species was explained through the differences in water vapor conductance between the three eggshell parts of the same egg (B, E, and P); (3) the technique was sensitive enough to detect significant differences between the three domestic species; (4) there was no overall significant difference between water vapor conductance of museum and fresh black-headed gull eggs; (5) there was no significant difference in water vapor conductance for egg fragments taken from the same egg both between different trials and within the same trial. We conclude, therefore, that this technique is an effective way of measuring interspecific water vapor conductance from eggshell fragments and that museum eggs are a suitable resource for such work.

Solo and duet calling in the pheasant coucal: sex and individual call differences in a nesting cuckoo with reversed size dimorphism

Duetting and female vocalisations have rarely been studied in tropical non-passerines. In coucals, a subfamily of nesting cuckoos, these behaviours have evolved under unusual conditions of male-biased parental care and reversed sexual size dimorphism. Here we provide the first detailed description of the structure and occurrence of sex-specific calls and duets in a monogamous coucal species, the pheasant coucal, Centropus phasianinus. Pheasant coucals of either sex use two types of far-reaching (>1 km) calls in their solo and duet displays: the ‘descending whoops’ call and, less frequently (25%), ‘scale’ calls. Both calls are series of very deep hooting notes that the larger females produce at lower frequency than the males (~326 versus 480 Hz). Descending whoops calls also vary among individuals but this difference is not consistent enough for individual identification. Most duets (63%) comprise a single scale call by each partner and the sexes start duets with equal frequency. Duetting triggers neighbouring pairs to duet too, suggesting a role in territory defence. Calling is most intense in the morning and early in the breeding season. The cryptic behaviour of coucals makes their calls an important tool for studies on their mating system, survey work and taxonomic research.