The mechanistic,genetic and evolutionary causes of bird eye colour variation

Birds display a rainbow of eye colours, but this trait has been little studied compared with plumage coloration. Avian eye colour variation occurs at all phylogenetic scales: it can be conserved throughout whole families or vary within one species, yet the evolutionary importance of this eye colour variation is under-studied. Here, we summarize knowledge of the causes of eye colour variation at three primary levels: mechanistic, genetic and evolutionary. Mechanistically, we show that avian iris pigments include melanin and carotenoids, which also play major roles in plumage colour, as well as purines and pteridines, which are often found as pigments in non-avian taxa. Genetically, we survey classical breeding studies and recent genomic work on domestic birds that have identified potential ‘eye colour genes’, including one associated with pteridine pigmentation in pigeons. Finally, from an evolutionary standpoint, we present and discuss several hypotheses explaining the adaptive significance of eye colour variation. Many of these hypotheses suggest that bird eye colour plays an important role in intraspecific signalling, particularly as an indicator of age or mate quality, although the importance of eye colour may differ between species and few evolutionary hypotheses have been directly tested. We suggest that future studies of avian eye colour should consider all three levels, including broad-scale iris pigment analyses across bird species, genome sequencing studies to identify loci associated with eye colour variation, and behavioural experiments and comparative phylogenetic analyses to test adaptive hypotheses. By examining these proximate and ultimate causes of eye colour variation in birds, we hope that our review will encourage future research to understand the ecological and evolutionary significance of this striking avian trait.     

Comparing plumage colour measurements obtained directly from live birds and from collected feathers: the case of the great tit Parus major

Birds frequently display a colourful plumage which is important both in inter and intraespecific communication, and either in sexual and social contexts. In last years some methodologies have been developed to, analyse plumage coloration, but the use of the spectrometers has been particularly important for UV range. Measurement of plumage coloration with the spectrometer may be taken directly on the bird or, alternatively by collecting some feathers and measuring them later in the laboratory. However, few is known about the reliability of measures obtained from feathers and whether these are really representative of plumage coloration. We tested this assumption analysing measurements of carotenoids-based coloration components (lightness, chroma and hue) and lutein peak of the yellow breast of the great tit Parus major. We used two spectrometers (Ocean optics and Minolta) which calculate differently the colour components. Our results showed that direct measurement of bird was highly repeatable to determine lightness, chroma and hue for both spectrometers. Similar results we found for collected feathers procedure for both devices. Collected feathers provided high representative measurements of colour values with Minolta spectrometer. Lightness was highly repeatable when we used Ocean optic spectrometer, but chroma and hue were moderate. Lutein peak was also highly repeatable in all cases. The number of feathers used to measure plumage coloration in collected feathers procedure strongly influenced values of colour plumage variables. In general, values of lightness, chroma and hue stabilised when more than 10–15 feathers were used although we found slight differences between spectrometers. However, only four feathers were needed for lutein peak. Thus, our results stress the need to use a minimum number of feathers in measuring plumage coloration from collected feathers.     

Why do melanin ornaments signal individual quality? Insights from metal element analysis of barn owl feathers

Melanin-based variation in colour patterns is under strong genetic control and not, or weakly, sensitive to the environment and body condition. Current signalling theory predicts that such traits may not signal honestly phenotypic quality because their production does not entail a significant fitness cost. However, recent studies revealed that in several bird species melanin-based traits covary with phenotypic attributes. In a first move to understand whether such covariations have a physiological basis, we quantified concentrations of five chemical elements in two pigmented plumage traits in the barn owl (Tyto alba). This bird shows continuous variation from immaculate to heavily marked with black spots (plumage spottiness) and from dark reddish-brown to white (plumage coloration), two traits that signal various aspects of individual quality. These two traits are sexually dimorphic with females being spottier and darker coloured than males. We found an enhancement in calcium and zinc concentration within black spots compared with the unspotted feather parts. The degree to which birds were spotted was positively correlated with calcium concentration within spots, whereas the unspotted feather parts of darker reddish-brown birds were more concentrated in zinc. This suggests that two different pigments are responsible for plumage spottiness and plumage coloration. We discuss the implications of our results in light of recent experimental field studies showing that female spottiness signals offspring humoral response towards an artificially administrated antigen, parasite resistance and fluctuating asymmetry of wing feathers.An erratum to this article can be found at     

Seasonal Changes in Colour: A Comparison of Structural,Melanin- and Carotenoid-Based Plumage Colours

Background

Plumage coloration is important for bird communication, most notably in sexual signalling. Colour is often considered a good quality indicator, and the expression of exaggerated colours may depend on individual condition during moult. After moult, plumage coloration has been deemed fixed due to the fact that feathers are dead structures. Still, many plumage colours change after moult, although whether this affects signalling has not been sufficiently assessed.

Methodology/Principal Findings

We studied changes in coloration after moult in four passerine birds (robin, Erithacus rubecula; blackbird, Turdus merula; blue tit, Cyanistes caeruleus; and great tit, Parus major) displaying various coloration types (melanin-, carotenoid-based and structural). Birds were caught regularly during three years to measure plumage reflectance. We used models of avian colour vision to derive two variables, one describing chromatic and the other achromatic variation over the year that can be compared in magnitude among different colour types. All studied plumage patches but one (yellow breast of the blue tit) showed significant chromatic changes over the year, although these were smaller than for a typical dynamic trait (bill colour). Overall, structural colours showed a reduction in relative reflectance at shorter wavelengths, carotenoid-based colours the opposite pattern, while no general pattern was found for melanin-based colours. Achromatic changes were also common, but there were no consistent patterns of change for the different types of colours.

Conclusions/Significance

Changes of plumage coloration independent of moult are probably widespread; they should be perceivable by birds and have the potential to affect colour signalling.     

Using colour spectral data in studies of geographic variation and taxonomy of birds: examples with two hummingbird genera, Anthracothorax and Eulampis

I propose a methodology to obtain and compare integral information on bird plumage coloration, using colour spectral data to conduct studies on geographic variation and taxonomy of different bird groups. I used principal component analysis and discriminant function analysis to compare groups of individuals by plumage coloration. As examples of the application of the methodology, I compared populations within the genus Eulampis and Anthracothorax. The results indicate possible taxonomic inadequacies and reveal situations that deserve further analysis, demonstrating the potential of the methodology in this area.Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird

Categorizing individuals into discrete forms in colour polymorphic species can overlook more subtle patterns in coloration that can be of functional significance. Thus, quantifying inter-individual variation in these species at both within- and between-morph levels is critical to understand the evolution of colour polymorphisms. Here we present analyses of inter-individual colour variation in the Reunion grey white-eye (Zosterops borbonicus), a colour polymorphic wild bird endemic to the island of Reunion in which all highland populations contain two sympatric colour morphs, with birds showing predominantly grey or brown plumage, respectively. We first quantified colour variation across multiple body areas by using a continuous plumage colour score to assess variation in brown-grey coloration as well as smaller scale variation in light patches. To examine the possible causes of among-individual variation, we tested if colour variation in plumage component elements could be explained by genotypes at two markers near a major-effect locus previously related to back coloration in this species, and by other factors such as age, sex and body condition. Overall, grey-brown coloration was largely determined by genetic factors and was best described by three distinct clusters that were associated to genotypic classes (homozygotes and heterozygote), with no effect of age or sex, whereas variation in smaller light patches was primarily related to age and sex. Our results highlight the importance of characterizing subtle plumage variation beyond morph categories that are readily observable since multiple patterns of colour variation may be driven by different mechanisms, have different functions and will likely respond in different ways to selection.     

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.     

Variation in plumage colour of the Great tit Parus major in relation to habitat, season and food

The plumage colour of nestling and adult Great tits Parus major major L. was studied at Trondheim (63 °N, 10 °E), Norway. Nestlings reared in deciduous woodland were yellower than those reared in coniferous woodland, those reared in 1983 were yellower than those in 1982, and the later in the breeding season they were reared the more yellow they were. Furthermore, adults were yellower than nestlings, and for both groups the males were yellower than the females. Experimental interchange of eggs between nests showed that the variation in plumage colour observed between broods was related primarily to the food and not to genetic differences. Sampling, by the neck-collar method, of the food brought by the parent birds showed that the yellower nestlings received a greater proportion of lepidopteran larvae, in particular greenish-coloured ones, than did the nestlings with a paler plumage. A speculation is whether or not the variation in plumage colour has some adaptive value (viz. background matching).
In avian systematics, plumage coloration has been used to distinguish and describe subspecies. The present study shows that such a classification should only be made with certain reservations, until possible variation in the food quality of the subspecies is known to have no influence on plumage coloration.     

The reliability of achromatic displays is island-dependent in nocturnal Storm Petrels

Nocturnal birds rely on achromatic visual signals to assess rivals and potential mates, but variation in the expression of these displays has been understudied. Here we use UV-visible reflectance spectrometry to study colour variation and the potential signalling function of the dark brown chest and white rump plumage – a colour pattern conspicuously exhibited during twilight courtship displays – in nocturnal Mediterranean Storm Petrels Hydrobates pelagicus melitensis from three islands with different exposures to predation and human disturbance. Human activity may increase perceived predation risk and thus affect activity budgets and the physiological stress response, with possible consequences on the relationship between individual body condition and plumage coloration. We found that chest and especially rump feathers reflected in the ultraviolet (UV) but there was no evidence of sexual dichromatism. However, we found support for a male-specific signalling role of plumage coloration. Indeed, chest yellow–red chroma and rump UV chroma were positively related to body condition in males, but only in the two islands representing the poorer environmental conditions. Therefore, environmental variability can potentially modify the reliability of achromatic displays, with possible consequences on sexual selection patterns in a nocturnal bird.     

Carotenoid‐based bill coloration functions as a social,not sexual,signal in songbirds (Aves: Passeriformes)

Many animals use coloration to communicate with other individuals. Although the signalling role of avian plumage colour is relatively well studied, there has been much less research on coloration in avian bare parts. However, bare parts could be highly informative signals as they can show rapid changes in coloration. We measured bill colour (a ubiquitous bare part) in over 1600 passerine species and tested whether interspecific variation in carotenoid‐based coloration is consistent with signalling to potential mates or signalling to potential rivals in a competitive context. Our results suggest that carotenoid bill coloration primarily evolved as a signal of dominance, as this type of coloration is more common in species that live in social groups in the nonbreeding season, and species that nest in colonies; two socio‐ecological conditions that promote frequent agonistic interactions with numerous and/or unfamiliar individuals. Additionally, our study suggests that carotenoid bill coloration is independent of the intensity of past sexual selection, as it is not related to either sexual dichromatism or sexual size dimorphism. These results pose a significant challenge to the conventional view that carotenoid‐based avian coloration has evolved as a developmentally costly, condition‐dependent sexual signal. We also suggest that bare part ornamentation may often signal different information than plumage ornaments.     

Plumage coloration can be perceived as a multiple condition‐dependent signal by Great Tits Parus major

The evolution of multiple signals can be explained because they enhance the perception of a general message by recipients. Plumage coloration frequently acts as a condition‐dependent signal, so that species displaying different colour patches have the potential to transmit information on condition through a multiple signalling system. The Great Tit Parus major exhibits plumage colour patches generated by the main types of colour production, some of which, particularly those based on melanins and carotenoids, are known to be related to body condition. However, the colour expressions of all of the different colour types have never been investigated simultaneously to determine whether they function as multiple signals of condition. In addition, visual perception models have never been applied to a multiple signalling system in a wild population of birds. Here I present information that links body condition with the colour expression of almost all of the different plumage patches of male Great Tits captured during the winter. Birds in better condition had greater reflectance values at short wavelengths in all plumage patches, and this was especially so in the white (i.e. structural) colour of the cheeks. Plumage colour characteristics were calculated by means of avian visual models, suggesting that Great Tits have the capacity to perceive information contained in the plumage coloration of conspecifics. These results show that short‐wavelength reflectance has great potential to transmit biologically significant information on the body condition of birds, even in achromatic plumage patches.     

Interspecific variation in the use of carotenoid-based coloration in birds: diet, life history and phylogeny

Birds show striking interspecific variation in their use of carotenoid-based coloration. Theory predicts that the use of carotenoids for coloration is closely associated with the availability of carotenoids in the diet but, although this prediction has been supported in single-species studies and those using small numbers of closely related species, there have been no broad-scale quantitative tests of the link between carotenoid coloration and diet. Here we test for such a link using modern comparative methods, a database on 140 families of birds and two alternative avian phylogenies. We show that carotenoid pigmentation is more common in the bare parts (legs, bill and skin) than in plumage, and that yellow coloration is more common than red. We also show that there is no simple, general association between the availability of carotenoids in the diet and the overall use of carotenoid-based coloration. However, when we look at plumage coloration separately from bare part coloration, we find there is a robust and significant association between diet and plumage coloration, but not between diet and bare part coloration. Similarly, when we look at yellow and red plumage colours separately, we find that the association between diet and coloration is typically stronger for red coloration than it is for yellow coloration. Finally, when we build multivariate models to explain variation in each type of carotenoid-based coloration we find that a variety of life history and ecological factors are associated with different aspects of coloration, with dietary carotenoids only being a consistent significant factor in the case of variation in plumage. All of these results remain qualitatively unchanged irrespective of the phylogeny used in the analyses, although in some cases the precise life history and ecological variables included in the multivariate models do vary. Taken together, these results indicate that the predicted link between carotenoid coloration and diet is idiosyncratic rather than general, being strongest with respect to plumage colours and weakest for bare part coloration. We therefore suggest that, although the carotenoid-based bird plumage may a good model for diet-mediated signalling, the use of carotenoids in bare part pigmentation may have a very different functional basis and may be more strongly influenced by genetic and physiological mechanisms, which currently remain relatively understudied.     

Covariation between plumage colour polymorphism and diet in the Barn Owl Tyto alba

Several hypotheses might explain the evolution and maintenance of colour morphs within animal populations. The 'alternative foraging strategy' hypothesis states that alternative colour morphs exploit different ecological niches. This hypothesis predicts that morphs differ in diet, either because foraging success on alternative prey species is morph-dependent or because differently coloured individuals exploit alternative habitats. I examined this prediction in the Barn Owl Tyto alba , a bird that varies in plumage coloration continuously from dark reddish-brown to white. On the European continent, Owls are light-coloured (subspecies T. a. alba ) in the south and reddish-brown ( T. a. guttata ) in the north; in central Europe the two subspecies interbreed, generating many colour variants. If plumage coloration indicates alternative foraging strategies, in sympatry dark- and light-coloured owls should consume prey species that are typical of the diets of T. a. guttata and T. a. alba in allopatry, respectively. In line with this prediction, both in allopatry and in sympatry in Switzerland T. a. guttata fed primarily upon Common Voles Microtus arvalis and T. a. alba upon Wood Mice Apodemus spp. Statistical analyses suggest that morph-dependent diet did not arise from a non-random habitat distribution of owls with respect to plumage coloration. This suggests that foraging success upon alternative prey is morph-dependent.     

Analysis from avian visual perspective reveals plumage colour differences among females of capuchino seedeaters (Sporophila)

Females of the closely related capuchino seedeaters are difficult to distinguish from one another based on human visual perception of colouration and morphology. We examined plumage colour differences among females of four species, the tawny‐bellied seedeater Sporophila hypoxantha, the dark‐throated seedeater S. ruficollis, the rufous‐rumped seedeater S. hypochroma, and the chesnut‐bellied seedeater S. cinnamomea. Reflectance values were measured on museum skins, and interspecific differences were analyzed using the Vorobyev‐Osorio avian colour discrimination model. Interspecific distances in the colour space calculated by the model were considerably higher than the threshold for colour discrimination, indicating the presence of colour differences among species that should be detectable by birds. Colour differences between S. hypoxantha and the other three species were the largest. A Discriminant Function Analysis showed that UV‐wavelength was particularly important in species separation. Our results indicate that female plumage of these four species is considerably divergent in colour; these differences being imperceptible to the human eye, thus representing previously unknown morphological evolution in these species.     

Elevational plumage divergence in the Rufous-capped Babbler (Cyanoderma ruficeps) on a mountainous island

Environment plays an important role in the evolution of plumage coloration in birds and may also lead to sexual dichromatism if males and females face different selection pressures. Mountains exhibit varying ecological conditions along their elevation gradient that may impose divergent selection on elevationally widespread species, causing intraspecific plumage divergence. For example, UV light environments often vary between montane and lowland habitats, which could potentially cause differences in plumage UV reflection between birds occurring in the two types of habitats. However, few studies have examined the effects of elevation on plumage evolution. In this study, we quantified the plumage coloration of the Rufous-capped Babbler Cyanoderma ruficeps from montane and lowland habitats on a mountainous island, Taiwan. We aimed to examine whether their plumage showed differences associated with changing ecological environments across the elevational gradient. The results supported that the plumage of babblers occupying montane habitats had higher UV-reflectance and brightness than that of lowland birds, corresponding to the higher UV intensity in montane than lowland background light environments. The elevational differences were mainly found across the ventral parts of babblers that had relatively higher levels of UV reflectance compared with their dorsal parts. Alternatively, the brighter plumage, with higher UV-reflectance in montane than lowland birds, might be mediated by physiological adaptation to other ecological factors, such as parasite pressures. The elevational differences in plumage UV-reflectance and brightness were more dramatic in males than in females. However, we found significant sexual dichromatism in different body parts between montane and lowland babblers in which females had brighter or stronger UV-associated coloration than males, suggesting that sexual selection has little impact on babbler plumage. Our study suggests the importance of elevational divergent selection associated with UV light or other ecological environments on avian plumage evolution.     

Contemporary divergence of island bird plumage

Although the diversity in avian plumage coloration is striking, there is little known about the rate with which colour diverges. Eastern bluebirds Sialia sialis bermudensis on the island of Bermuda are considered endemic based upon differences in coloration from the mainland, but recent molecular evidence suggests they established on the island only 400 yr ago. We explored sexual dichromatism and colour divergence in this isolated population, thus providing one of the few quantitative accounts of contemporary plumage change. Contrary to expectations that sexual dichromatism would decrease in this sedentary island population, we found that males and females have increased plumage ornamentation in a coordinated fashion that acts to preserve sexual dichromatism, while plumage colour is also altered to become brighter and bluer. These differences were in place at least 100 yr ago based upon a separate analysis of museum specimens. Our results provide insight into the divergence of plumage colour in an incipient species, and we show the remarkable extent to which plumage colour can change over contemporary time frames.     

Informative content of melanin‐based plumage colour in adult Eurasian kestrels

Covariation between melanin‐based colorations and other phenotypic attributes has been rarely measured simultaneously in males and females. Such covariations and mechanisms mediating them have crucial importance determining the signalling function of these coloured ornaments in the two sexes. We examined the role of four melanin‐based coloured plumage patches as indicators of quality in both males and females of the sexually dimorphic and dichromatic Eurasian kestrel Falco tinnunculus. Previous kestrel studies have focused on the size of melanin plumage patches in either males or females as indicators of individual quality. Here, we used spectrophotometric measurements of three plumage patches and the size of another plumage patch to investigate the information content of multiple plumage colour traits in male and female kestrels. We found that females with bright plumage in the head and with high UV chroma in black parts of the rump showed good body condition and innate immunity. In addition, laying date was significantly explained by the intensity of the brown in the head of females. Meanwhile, in males we only found that individuals with greyer rumps showed better innate immunity. Altogether, our results indicate that, irrespective of the mechanism promoting covariation between coloration and individual quality, melanin‐based coloration can inform on individual quality in adult kestrels.     

Morphological and plumage colour variation in the Réunion grey white‐eye (Aves: Zosterops borbonicus): assessing the role of selection

The Réunion grey white‐eye (Zosterops borbonicus), a small passerine endemic to the island of Réunion (Mascarene archipelago), constitutes an extraordinary case of phenotypic variation within a bird species, with conspicuous plumage colour differentiation at a microgeographical scale. To understand whether natural selection could explain such variability, we compared patterns of variation in morphological and plumage colour traits within and among populations. To quantify morphological variation, we used measurements obtained by Frank Gill in the 1960s from 239 individuals collected in 60 localities distributed over the entire island of Réunion. To quantify colour variation, we measured the reflectance spectra of plumage patches of 50 males from a subset of Gill's specimens belonging to the five recognized plumage colour variants and used a visual model to project these colours in an avian‐appropriate, tetrachromatic, colour space. We found that variants occupy different regions of the avian colour space and that between‐variant differences for most plumage patches could be discriminated by the birds. Differences in morphology were also detected, but these were, in general, smaller than colour differences. Overall, we found that variation in both plumage colour and morphology among variants is greater than would be expected if genetic drift alone was responsible for phenotypic divergence. As the plumage colour variants correspond to four geographical forms, our results suggest that phenotypic evolution in the Réunion grey white‐eye is at least partly explained by divergent selection in different habitats or regions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 459–473.     

Uncorrelated evolution between vocal and plumage coloration traits in the trogons: a comparative study

The costs of bird song incurred in a diversity of ways may result in trade‐offs in the production and maintenance of elaborate plumage ornaments. In this paper, we examine evolutionary trade‐offs between acoustic and visual signalling in trogon birds (Trogonidae). Using multiple regressions with phylogenetically independent contrasts, we found that interspecific variation in male plumage coloration was not significantly predicted by song traits (reduced by PCA) or altitude. Although plumage coloration is expected to decrease with increases in song elaboration, both groups of variables were not related. Given that song and plumage coloration traits are likely targets of sexual selection, we also examined their relationships with sexual plumage dimorphism. We found that male carotenoid‐derived coloration was positively related to sexual plumage dimorphism, suggesting that sexual selection on male carotenoid‐derived coloration may be stronger than on melanin‐ or structurally based coloration, or than on acoustic traits. Comparative studies on other bird families accounting for the effects of phylogeny as well as environmental covariates are required to test the generality of our findings in trogons.     

Female‐ and male‐specific signals of quality in the barn owl

Most bird studies of female signalling have been confined to species in which females display a male‐ornament in a vestigial form. However, a great deal of benefit may be gained from considering phenotypic traits that are specific to females. This is because (1) sex‐specific traits may signal sex‐specific qualities and (2) females may develop a male‐ornament not because they are selected to do so, but because fathers transmit to daughters the underlying genes for its expression (genetic correlation between the sexes). We investigated these two propositions in the barn owl Tyto alba, a species in which male plumage is lighter in colour and less marked with black spots than that of females. Firstly, we present published evidence that female plumage spottiness reflects parasite resistance ability. We also show that male plumage coloration is correlated with reproductive success, male feeding rate and heart mass. Secondly, cross‐fostering experiments demonstrate that plumage coloration and spottiness are genetically correlated between the sexes. This implies that if a given trait value is selected in one sex, the other sex will indirectly evolve towards a similar value. This prediction is supported by the observation that female plumage coloration and spottiness resembled that of males, in comparisons at the level of Tyto alba alba populations, Tyto alba subspecies and Tyto species. Our results therefore support the hypothesis that sex‐specific traits signal sex‐specific qualities and that a gene for a sex‐specific trait can be expressed in the other sex as the consequence of a genetic correlation between the sexes.