Multiple shifts between violet and ultraviolet vision in a family of passerine birds with associated changes in plumage coloration

Colour vision in diurnal birds falls into two discrete classes, signified by the spectral sensitivity of the violet- (VS) or ultraviolet-sensitive (UVS) short wavelength-sensitive type 1 (SWS1) single cone. Shifts between sensitivity classes are rare; three or four are believed to have happened in the course of avian evolution, one forming UVS higher passerines. Such shifts probably affect the expression of shortwave-dominated plumage signals. We have used genomic DNA sequencing to determine VS or UVS affinity in fairy-wrens and allies, Maluridae, a large passerine family basal to the known UVS taxa. We have also spectrophotometrically analysed male plumage coloration as perceived by the VS and UVS vision systems. Contrary to any other investigated avian genus, Malurus (fairy-wrens) contains species with amino acid residues typical of either VS or UVS cone opsins. Three bowerbird species (Ptilonorhynchidae) sequenced for outgroup comparison carry VS opsin genes. Phylogenetic reconstructions render one UVS gain followed by one or more losses as the most plausible evolutionary scenario. The evolution of avian ultraviolet sensitivity is hence more complex, as a single shift no longer explains its distribution in Passeriformes. Character correlation analysis proposes that UVS vision is associated with shortwave-reflecting plumage, which is widespread in Maluridae.     

Ultraviolet vision in birds: the importance of transparent eye media

Ultraviolet (UV)-sensitive visual pigments are widespread in the animal kingdom but many animals, for example primates, block UV light from reaching their retina by pigmented lenses. Birds have UV-sensitive (UVS) visual pigments with sensitivity maxima around 360–373 nm (UVS) or 402–426 nm (violet-sensitive, VS). We describe how these pigments are matched by the ocular media transmittance in 38 bird species. Birds with UVS pigments have ocular media that transmit more UV light (wavelength of 50% transmittance, λ_T0.5, 323 nm) than birds with VS pigments (λ_T0.5, 358 nm). Yet, visual models predict that colour discrimination in bright light is mostly dependent on the visual pigment (UVS or VS) and little on the ocular media. We hypothesize that the precise spectral tuning of the ocular media is mostly relevant for detecting weak UV signals, e.g. in dim hollow-nests of passerines and parrots. The correlation between eye size and UV transparency of the ocular media suggests little or no lens pigmentation. Therefore, only small birds gain the full advantage from shifting pigment sensitivity from VS to UVS. On the other hand, some birds with VS pigments have unexpectedly low UV transmission of the ocular media, probably because of UV blocking lens pigmentation.     

The contribution of single and double cones to spectral sensitivity in budgerigars during changing light conditions

Bird colour vision is mediated by single cones, while double cones and rods mediate luminance vision in bright and dim light, respectively. In daylight conditions, birds use colour vision to discriminate large objects such as fruit and plumage patches, and luminance vision to detect fine spatial detail and motion. However, decreasing light intensity favours achromatic mechanisms and eventually, in dim light, luminance vision outperforms colour vision in all visual tasks. We have used behavioural tests in budgerigars (Melopsittacus undulatus) to investigate how single cones, double cones and rods contribute to spectral sensitivity for large (3.4°) static monochromatic stimuli at light intensities ranging from 0.08 to 63.5 cd/m². We found no influences of rods at any intensity level. Single cones dominate the spectral sensitivity function at intensities above 1.1 cd/m², as predicted by a receptor noise-limited colour discrimination model. Below 1.1 cd/m², spectral sensitivity is lower than expected at all wavelengths except 575 nm, which corresponds to double cone function. We suggest that luminance vision mediated by double cones restores visual sensitivity when single cone sensitivity quickly decreases at light intensities close to the absolute threshold of colour vision.     

Physical Alignments Between Plumage Carotenoid Spectra and Cone Sensitivities in Ultraviolet-Sensitive (UVS) Birds (Passerida: Passeriformes)

Among birds, single cone sensitivities responsible for color vision appear surprisingly conserved even though chromatic signals vary greatly. Thus it is widely held that avian visual signal and receptor characteristics are rarely aligned. Analysis of a diverse passerine clade (Passerida) with characteristically ultraviolet-sensitive (UVS) vision revealed that plumage carotenoid reflectance spectra matched cone maximal sensitivities at several levels: (1) plumage carotenoid reflectance minima and maxima in aggregate aligned with the four UVS single cones; (2) the corresponding reflectance features of yellow (hydroxy- and ε-keto) and red (3- and 4-β-keto) carotenoid classes aligned with different combinations of cones; (3) pairs of reflectance features (e.g. one minimum and one maximum) of each carotenoid class aligned with pairs of (opponent) cones that evoke chromatic perception; (4) passerid plumage carotenoids aligned more closely to their own (UVS) visual system than to the distinctive homologous cone classes of the violet-sensitive system found in other birds. The ubiquitous occurrence of plumage carotenoids ipso facto demonstrates that alignments of avian visual signals and receptors are widespread, and provides novel evidence that carotenoids are important to avian communication. Moreover, alignment of different physical spectra to different cone combinations in a fixed receptor array provides a straightforward mechanism that accommodates signal diversity within the context of a relatively conserved visual system. The distinct patterns of variation and alignment observed for yellow versus red carotenoids further suggest that these pigment classes convey different physical aspects of content, which may foster carotenoid-based plumage diversity through signal design trade-offs.     

Contrast versus colour in aposematic signals

Conspicuousness is an important feature of warning coloration. One hypothesis for its function is that it increases signal efficacy by facilitating avoidance learning. An alternative, based on the handicap hypothesis, suggests that the degree of conspicuousness holds information directly about the quality of the prey, and that predators associate and learn about the conspicuousness of the coloration, and not the actual colour pattern. We studied the relative importance of signal contrast and the colours of signals for predator attention during discrimination. We used young chicks, Gallus gallus domesticus, as predators and small blue or red paper cones on either matching or contrasting paper backgrounds as stimuli associated with palatable or unpalatable chick crumbs. In four treatment groups, birds could use either cone and/or background colour, cone colour only, background colour only or cone-to-background contrast as cues for discrimination. Only birds in the contrast treatment failed to learn their discrimination task. Birds that had a choice between cone and background colour as cues used the cone colour and they learned the task faster than did birds that had to use background colour as a cue. The results suggest that birds primarily attend to the colours of signals and disregard contrast in discrimination tasks; they thus fail to support a handicap function of conspicuous aposematic coloration. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Concerted Shifts in Absorption Maxima of Yellow and Red Plumage Carotenoids Support Specialized Tuning of Chromatic Signals to Different Visual Systems in Near-Passerine Birds

Recent evidence that absorption maxima (λR_min) expressed by colorful plumage pigments align to diagnostic cone sensitivities of affiliated visual systems suggests that birds employ specialized signals in relation to their color vision. However, these studies compared different pigments and clades for the violet (porphyrins in non-passerines) and ultraviolet (carotenoids in passerines) sensitive system, which confounds chemistry and phylogeny with tuning patterns. To test whether signal alignments to violet (VS) and ultraviolet (UVS) systems transcend confounding factors, parallel analyses were conducted for a diversity of near-passerines, a group in which plumage carotenoids occur in taxa with either visual system. Conventional and phylogenetically informed analyses confirmed earlier findings: short wavelength absorbing (yellow carotenoid) pigments aligned λR_min with the violet-sensitive (V) cone of VS species but with the short wavelength-sensitive (S) cone of UVS species, whereas long wavelength-absorbing (red carotenoid) pigments aligned only with the S cone of VS species. More extensive variation among VS yellow carotenoids produced λR_min alignments to cone sensitivities that differed at shorter (peaks) versus longer (overlaps) wavelengths. Ancestral trait reconstructions indicated that signals evolved to match pre-existing VS systems, but did not resolve scenarios for UVS systems. Regardless of historical details, alignments expressed a higher-level pattern in which λR_min values were blue-shifted for yellow and red carotenoids in VS compared to UVS species, a pattern opposite that expressed by receptor sensitivities between systems. Thus, generalized functional designs attributed to avian color vision allow for specialized visual communication through the development of chromatic signals suited to each perceptual system.     

Nestling colouration is adjusted to parent visual performance in altricial birds

Hitherto, most of the investigation on the perceptual efficacy of begging signals has dwelled on how patterns of nestling colouration adjust to predominant nest luminosity. However, visual sensitivity of birds varies across species, which raises the question of whether colouration of traits involved in begging displays is adjusted to parent visual capacities. Here, by comparing nestling colouration and visual sensitivity across 22 altricial bird species, we provide a first test of this hypothesis. Firstly, we assessed differences in performance of typical UV‐tuned and violet‐tuned bird eyes when looking at the nestling traits under the light regimes prevailing at their nests. Secondly, while controlling for common ancestry in a comparative approach, we explored variation in colouration of nestlings in relation to parent visual system. The colour discrimination model indicated a general higher performance of the ultraviolet over the violet eye at detecting gape and body skin traits in either open‐ or hole‐nest light conditions. Gape colouration was associated with parental visual system as the nestlings of UVS species displayed more yellow and less pure ultraviolet mouths than the nestlings of VS species. Thus, our results agree with an adaptive parent–offspring communication scenario where the nestlings’ colours tuned the perception capacities of their parents.     

Bat Eyes Have Ultraviolet-Sensitive Cone Photoreceptors

Mammalian retinae have rod photoreceptors for night vision and cone photoreceptors for daylight and colour vision. For colour discrimination, most mammals possess two cone populations with two visual pigments (opsins) that have absorption maxima at short wavelengths (blue or ultraviolet light) and long wavelengths (green or red light). Microchiropteran bats, which use echolocation to navigate and forage in complete darkness, have long been considered to have pure rod retinae. Here we use opsin immunohistochemistry to show that two phyllostomid microbats, Glossophaga soricina and Carollia perspicillata, possess a significant population of cones and express two cone opsins, a shortwave-sensitive (S) opsin and a longwave-sensitive (L) opsin. A substantial population of cones expresses S opsin exclusively, whereas the other cones mostly coexpress L and S opsin. S opsin gene analysis suggests ultraviolet (UV, wavelengths <400 nm) sensitivity, and corneal electroretinogram recordings reveal an elevated sensitivity to UV light which is mediated by an S cone visual pigment. Therefore bats have retained the ancestral UV tuning of the S cone pigment. We conclude that bats have the prerequisite for daylight vision, dichromatic colour vision, and UV vision. For bats, the UV-sensitive cones may be advantageous for visual orientation at twilight, predator avoidance, and detection of UV-reflecting flowers for those that feed on nectar.     

Rapid evolution of elaborate male coloration is driven by visual system in Australian fairy‐wrens (Maluridae)

The interplay between colour vision and animal signalling is of keen interest to behavioural ecologists and evolutionary biologists alike, but is difficult to address in terrestrial animals. Unlike most avian lineages, in which colour vision is relatively invariant among species, the fairy‐wrens and allies (Maluridae) show a recent gain of ultraviolet sensitivity (UVS). Here, we compare the rates of colour evolution on 11 patches for males and females across Maluridae in the context of their visual system. We measured reflectance spectra for 24 species, estimating five vision‐independent colour metrics as well as metrics of colour contrast among patches and sexual dichromatism in a receiver‐neutral colour space. We fit Brownian motion (BM) and Ornstein–Uhlenbeck (OU) models to estimate evolutionary rates for these metrics and to test whether male coloration, female coloration or dichromatism was driven by selective regimes defined by visual system or geography. We found that in general male coloration evolved rapidly in comparison with females. Male colour contrast was strongly correlated with visual system and expanded greatly in UVS lineages, whereas female coloration was weakly associated with geography (Australia vs. Papua New Guinea). These results suggest that dichromatism has evolved in Maluridae as males and females evolve at different rates, and are driven by different selection pressures.     

The UV visual world of fishes: a review

Ultraviolet-A radiation (320–400 nm) is scattered rapidly in water. Despite this fact, UV is present in biologically useful amounts to at least 100 m deep in clear aquatic environments. Discovery of UV visual pigments with peak absorption at around 360 nm in teleost cone photoreceptors indicates that many teleost fishes may be adapted for vision in the UV range. Considering the characteristic absorption curve for visual pigments, about 18% of the downwelling light that illuminates objects at 30-m depth would be available to UV-sensitive cones. Strong scattering of UV radiation should produce unique imaging conditions as a very bright UV background in the horizontal view and a marked veiling effect that, with distance, obscures an image. Many teleosts have three, or even four, classes of cone cells mediating colour vision in their retina and one can be sensitive to UV. These UV-sensitive cones contain a visual pigment based on a unique opsin which is highly conserved between fish species. Several powerful methods exist for demonstration of UV vision, but all are rather demanding in terms of technique and equipment. Demonstration that the eye lacks UV-blocking compounds that are present in many fish eyes is a simpler method that can indicate the possibility of UV vision. The only experimental evidence for the use of UV vision by fishes is connected to planktivory: detection of UV-opaque objects at close range against a bright UV background is enhanced by the physical properties of UV light. Once present, perhaps for the function of detecting food, UV vision may well be co-opted through natural selection for other functions. Recent discovery that UV vision is critically important for mate choice in some birds and lizards is a strong object lesson for fish ecologists and behaviourists. Other possible functions amount to far more than merely adding a fourth dimension to the visible spectrum. Since UV is scattered so effectively in water, it may be useful for social signalling at short range and reduce the possibility of detection by other, illegitimate, receivers. Since humans are blind to UV light, we may be significantly in error, in many cases, in our attempts to understand and evaluate visual aspects of fish behaviour. A survey of the reflectance properties of skin pigments in fishes reveals a rich array of pigments with reflectance peaks in the UV. For example, the same yellow to our eyes may comprise two perceptually different colours to fish, yellow and UV-yellow. It is clearly necessary for us to anticipate that many fishes may have some form of UV vision.     

Studies on UV reflection in feathers of some 1000 bird species: are UV peaks in feathers correlated with violet‐sensitive and ultraviolet‐sensitive cones?

Nine hundred and sixty-eight bird species, covering all orders, were studied in search of distinctive ultraviolet reflections. All species in the following orders were completely surveyed: Struthioniformes, Tinamiformes, Craciformes, Turniciformes, Galbuliformes, Upupiformes, Coliiformes, Apodiformes and Musophagiformes. The coloured plumage regions in particular exhibited high proportions of UV-reflecting feathers. Bird orders with species which are believed to possess VS (violet-sensitive) cone types mostly had their UV maxima between 380 and 399 nm while orders with species which are assumed to have UVS (ultraviolet-sensitive) cone types contained significantly species which had their UV maxima between 300 and 379 nm. With an emphasis on non-passerine birds the present study provides evidence that birds of many more groups may see UV light than have been studied to date. Ecological aspects related to UV reflection and perception, as well as sexual dimorphism visible only in the UV, are discussed.     

Do bright colors at nests incur a cost due to predation?

Summary Birds show much interspecific variation in the coloration and brightness of their plumage. I examine the hypothesis that selection due to predation on incubating birds and their nest contents can explain part of this diversity. First, I argue that rather than using absolute rates of nest predation to make predictions about the costs of conspicuous colours, we should measure experimentally whether increases in plumage conspicuousness elevate rates of nest predation. Second, I present experimental data investigating the cost of red and brown colour at ground and tree nests. These data provide the first evidence that bright colours do attract predators to nests and that, in addition, this cost varies according to the nesting site. Natural selection seems to most strongly oppose the evolution of conspicuous colours in ground-nesting birds.     

The molecular evolution of avian ultraviolet- and violet-sensitive visual pigments

The shortwave-sensitive SWS1 class of vertebrate visual pigments range in lambda(max) from the violet (385-445 nm) to the ultraviolet (UV) (365-355 nm), with UV-sensitivity almost certainly ancestral. In birds, however, the UV-sensitive pigments present in a number of species have evolved secondarily from an avian violet-sensitive (VS) pigment. All avian VS pigments expressed in vitro to date encode Ser86 whereas Phe86 is present in all non-avian ultraviolet sensitive (UVS) pigments. In this paper, we show by site directed mutagenesis of avian VS pigments that Ser86 is required in an avian VS pigment to maintain violet-sensitivity and therefore underlies the evolution of avian VS pigments. The major mechanism for the evolution of avian UVS pigments from an ancestral avian VS pigment is undoubtedly a Ser90Cys substitution. However, Phe86, as found in the Blue-crowned trogon, will also short-wave shift the pigeon VS pigment into the UV whereas Ala86 and Cys86 which are also found in natural avian pigments do not generate short-wave shifts when substituted into the pigeon pigment. From available data on avian SWS1 pigments, it would appear that UVS pigments have evolved on at least 5 separate occasions and utilize 2 different mechanisms for the short-wave shift.     

The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.     

High sensitivity to short wavelengths in a lizard and implications for understanding the evolution of visual systems in lizards

Progress in developing animal communication theory is frequently constrained by a poor understanding of sensory systems. For example, while lizards have been the focus of numerous studies in visual signalling, we only have data on the spectral sensitivities of a few species clustered in two major clades (Iguania and Gekkota). Using electroretinography and microspectrophotometry, we studied the visual system of the cordylid lizard Platysaurus broadleyi because it represents an unstudied clade (Scinciformata) with respect to visual systems and because UV signals feature prominently in its social behaviour. The retina possessed four classes of single and one class of double cones. Sensitivity in the ultraviolet region (UV) was approximately three times higher than previously reported for other lizards. We found more colourless oil droplets (associated with UV-sensitive (UVS) and short wavelength-sensitive (SWS) photoreceptors), suggesting that the increased sensitivity was owing to the presence of more UVS photoreceptors. Using the Vorobyev-Osorio colour discrimination model, we demonstrated that an increase in the number of UVS photoreceptors significantly enhances a lizard's ability to discriminate conspecific male throat colours. Visual systems in diurnal lizards appear to be broadly conserved, but data from additional clades are needed to confirm this.     

Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines

Ultraviolet (UV) light-transmitted signals play a major role in avian foraging and communication, subserving functional roles in feeding, mate choice, egg recognition, and nestling discrimination. Sequencing functionally relevant regions of the short wavelength sensitive type 1 (SWS1) opsin gene that is responsible for modulating the extent of SWS1 UV sensitivity in birds allows predictions to be made about the visual system's UV sensitivity in species where direct physiological or behavioral measures would be impractical or unethical. Here, we present SWS1 segment sequence data from representative species of three avian lineages for which visually based cues for foraging and communication have been investigated to varying extents. We also present a preliminary phylogenetic analysis and ancestral character state reconstructions of key spectral tuning sites along the SWS1 opsin based on our sequence data. The results suggest ubiquitous ultraviolet SWS1 sensitivity (UVS) in both paleognaths, including extinct moa (Emeidae), and parrots, including the nocturnal and flightless kakapo (Strigops habroptilus), and in most, but not all, songbird (oscine) lineages, and confirmed violet sensitivity (VS) in two suboscine families. Passerine hosts of avian brood parasites were included both UVS and VS taxa, but sensitivity did not co-vary with egg rejection behaviors. The results should stimulate future research into the functional parallels between the roles of visual signals and the genetic basis of visual sensitivity in birds and other taxa.     

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.     

Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (<Emphasis Type="Italic">Sephanoides sephaniodes</Emphasis>)

We studied the photopic spectral sensitivity in the green-backed firecrown, Sephanoides sephaniodes, a South American hummingbird, and its possible ecological relationship with preferred flowers and body colouration. Avian colour vision is in general tetrachromatic with at least four types of cones, which vary in sensitivity from the near ultraviolet (UV) to the red wavelength range. Hummingbirds represent an important family of birds, yet little is known about their eye sensitivity, especially about the role of photoreceptors and their oil droplet complements. The photopic electroretinogram shows a main sensitivity peak at 560 nm and a secondary peak in the UV, and may be explained by the presence of four single cones (lambda (max) at ~370, 440, 508 and 560 nm), and a double cone (lambda (max) at 560 nm) screened by oil droplets. The flowers preferred by the firecrown are those in which the red-green wavelength region predominates and have higher contrast than other flowers. The crown plumage of males is highly iridescent in the red wavelength range (peak at 650 nm) and UV; when plotted in a high-dimensional tetrachromatic space, it falls in a "red + UV" purple hue line, suggesting a potential significant communication signal for sexual differentiation.     

Changes in carotenoid‐based plumage colour in relation to age in European Serins Serinus serinus

Yearling birds generally display duller colours than adults. This may be due to selection favouring birds with more intensely coloured plumage or to an increase in colour after the first complete moult. Most research to date on the topic has been carried out on species with structural plumage coloration or with carotenoid‐based coloration that is produced by the unmodified deposition of pigments. However, no study has been carried out on species whose carotenoids are metabolically modified before deposition. In this study, we assess age‐related changes in the carotenoid‐based coloration of European Serins, a species that metabolically processes carotenoids before they can be deposited into feathers. Birds were captured over consecutive years and we carried out both cross‐sectional and longitudinal analysis. Adults had significantly greater values of lightness and chroma than yearling birds. However, there were no changes in plumage colour when analysing the same individuals captured in subsequent seasons. Plumage lightness and chroma of adult males after moult were related to body mass, suggesting a role of body condition on plumage coloration. Our results suggest that changes in plumage coloration with age in European Serins are due to a selection process that favours more intensely coloured individuals.     

Divergent mechanisms for the tuning of shortwave sensitive visual pigments in vertebrates.

Of the four classes of vertebrate cone visual pigments, the shortwave-sensitive SWS1 class shows the shortest lambda(max) values with peaks in different species in either the violet (390-435 nm) or ultraviolet (around 365 nm) regions of the spectrum. Phylogenetic evidence indicates that the ancestral pigment was probably UV-sensitive (UVS) and that the shifts between violet and UV have occurred many times during evolution. This is supported by the different mechanisms for these shifts in different species. All visual pigments possess a chromophore linked via a Schiff base to a Lys residue in opsin protein. In violet-sensitive (VS) pigments, the Schiff base is protonated whereas in UVS pigments, it is almost certainly unprotonated. The generation of VS from ancestral UVS pigments most likely involved amino acid substitutions in the opsin protein that serve to stabilise protonation. The key residues in the opsin protein for this are at sites 86 and 90 that are adjacent to the Schiff base and the counterion at Glu113. In this review, the different molecular mechanisms for the UV or violet shifts are presented and discussed in the context of the structural model of bovine rhodopsin.