Variability in avian eggshell colour: a comparative study of museum eggshells

Abstract

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.

Figure 1. Avian eggshell colours.

(A) 3D diagram for all spectra (see methods) in an avian tetrachromatic colour opponent space following Kelber et al. . Boundaries are drawn following Cassey et al. and labels indicate whether colours reflect maximally in the ultraviolet- (UV), short- (SWS), medium- (MWS), or long-wavelength sensitive regions of the spectrum. (B) Average reflectance spectra for five representative eggs as represented in (C) for their replicate (n = 6) individual reflectance spectra plotted in the same 3D tetrachromatic space. (D) The eggs of the five representative avian species as photographed courtesy of the Natural History Museum, Tring, United Kingdom. Colours of the lines in (B) and the loci in (C) correspond to the text colours of the species labels in (D).

Figure 2. Taxonomic differences in relative reflectance spectra between sister species.

Boxplots (median, lower and upper quartiles, and one standard deviation below and above the mean) of the sum differences between reflectance spectra of sister taxa from varying taxonomic levels.

Figure 3. Taxonomic variability in the percentage reflectance of eggshell spectra.

Results from nested analysis of variance (nested ANOVA), at 5 nm steps across the wavelength. Coloured lines indicate the cumulative percentage of the variability that occurs between replicate measures within an egg (black line), between different eggs within a clutch (grey line), between different clutches within a species (blue line), between different species within a family (red line), and between different families (top black line).

Figure 4. Signal-to-noise ratio for average reflectance spectra.

Average (black line) and 5^th and 95^th percentiles (grey lines) at 5 nm steps across the wavelength, among the six replicate spectra across species with (A) immaculate, (B) partly maculated, and (C) heavily maculated eggshell types.

Figure 5. Taxonomic variability in perceived eggshell colour traits.

Percentages of variability among eggshell reflectance measures from nested analysis of variance (nested ANOVA), for luminance (brightness) and each of the three independent tetrachromatic axes (X, Y, Z), that occur between replicate measures within an egg, between different eggs within a clutch, between different clutches within a species, between different species within a family, and between different families.