Olle Håstad

Evolution of ultraviolet vision in the largest avian radiation - the passerines.

BackgroundInterspecific variation in avian colour vision falls into two discrete classes: violet sensitive (VS) and ultraviolet sensitive (UVS). They are characterised by the spectral sensitivity of the most shortwave sensitive of the four single cones, the SWS1, which is seemingly under direct control of as little as one amino acid substitution in the cone opsin protein. Changes in spectral sensitivity of the SWS1 are ecologically important, as they affect the abilities of birds to accurately assess potential mates, find food and minimise visibility of social signals to predators. Still, available data have indicated that shifts between classes are rare, with only four to five independent acquisitions of UV sensitivity in avian evolution.ResultsWe have classified a large sample of passeriform species as VS or UVS from genomic DNA and mapped the evolution of this character on a passerine phylogeny inferred from published molecular sequence data. Sequencing a small gene fragment has allowed us to trace the trait changing from one stable state to another through the radiation of the passeriform birds. Their ancestor is hypothesised to be UVS. In the subsequent radiation, colour vision changed between UVS and VS at least eight times.ConclusionsThe phylogenetic distribution of SWS1 cone opsin types in Passeriformes reveals a much higher degree of complexity in avian colour vision evolution than what was previously indicated from the limited data available. Clades with variation in the colour vision system are nested among clades with a seemingly stable VS or UVS state, providing a rare opportunity to understand how an ecologically important trait under simple genetic control may co-evolve with, and be stabilised by, associated traits in a character complex.

Pollinating birds differ in spectral sensitivity

Pollinating animals and their angiosperm hosts often show strong co-adaptation in traits that increase the likelihood of a successful transfer of pollen and nutrient rewards. One such adaptation is the reported colour difference caused by unequal distribution of anthocyanidin pigments amongst plant species visited by hummingbirds and passerines. This phenomenon has been suggested to reflect possible differences in the colour vision of these pollinating birds. The presence of any such difference in colour vision would arguably affect the ecological and evolutionary interactions between flowers and their visitors, accentuating differences in floral displays and attractiveness of plants to the favoured avian pollinators. We have tested for differences in colour vision, as indicated by the amino acid present at certain key positions in the short-wavelength-sensitive type 1 (SWS1) visual pigment opsin, between the major groups of pollinating birds: the non-passerine Trochilidae (hummingbirds), the passerine Meliphagidae (honeyeaters) and Nectariniidae (sunbirds) plus five other Passerida passerine families. The results reveal gross spectral sensitivity differences between hummingbirds and honeyeaters, on the one hand, and the Passerida species, on the other.

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 and foraging in dip and plunge diving birds

Many fishes are sensitive to ultraviolet (UV) light and display UV markings during courtship. As UV scatters more than longer wavelengths of light, these signals are only effective at short distances, reducing the risk of detection by swimming predators. Such underwater scattering will be insignificant for dip and plunge diving birds, which prey on fishes just below the water surface. One could therefore expect to find adaptations in the eyes of dip and plunge diving birds that tune colour reception to UV signals. We used a molecular method to survey the colour vision tuning of five families of dip or plunge divers and compared the results with those from sister taxa of other foraging methods. We found evidence of extended UV vision only in gulls (Laridae). Based on available evidence, it is more probable that this trait is associated with their terrestrial foraging habits rather than piscivory.

Rapid population divergence linked with co-variation between coloration and sexual display in strawberry poison frogs.

The likelihood of speciation is assumed to increase when sexually selected traits diverge together with ecologically important traits. According to sexual selection theory, the evolution of exaggerated display behavior is driven by increased mating success, but limited by natural selection, for example, through predation. However, the evolution of aposematic coloration (i.e., an ecologically important trait) could relieve the evolution of exaggerated display behavior from the bound of predation, resulting in joint divergence in aposematic coloration and sexual display behavior between populations. We tested this idea by examining conspicuousness, using color contrasts between individuals and their native backgrounds, and sexual display of 118 males from genetically diverged populations of the Strawberry poison frog, Dendrobates pumilio. Our results show that the level of conspicuousness of the population predicts the sexual display behavior of males. Males from conspicuous populations used more exposed calling sites. We argue that changes in aposematic coloration may rapidly cause not only postmating isolation due to poorly adapted hybrids, but also premating isolation through shifts in mating behaviors.

Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments

Recently, in vitro mutation studies have made it possible to predict the wavelengths of maximum absorbance (λmax) of avian UV/violet sensitive visual pigments (SWS1) from the identity of a few key amino acid residues in the opsin gene. Given that the absorbance spectrum of a cone’s visual pigment and of its pigmented oil droplet can be predicted from just the λmax, it may become possible to predict the entire spectral sensitivity of a bird using genetic samples from live birds or museum specimens. However, whilst this concept is attractive, it must be validated to assess the reliability of the predictions of λmax from opsin amino acid sequences. In this paper, we have obtained partial sequences covering three of the known spectral tuning sites in the SWS1 opsin and predicted λmax of all bird species for which the spectral absorbance has been measured using microspectrophotometry. Our results validate the use of molecular data from genomic DNA to predict the gross differences in λmax between the violet- and ultraviolet-sensitive subtypes of SWS1 opsin. Additionally, we demonstrate that a bird, the bobolink Dolichonyx oryzivorus L., can have more than one SWS1 visual pigment in its retina.

Different ranking of avian colors predicted by modeling of retinal function in humans and birds.

Only during the past decade have vision‐system‐neutral methods become common practice in studies of animal color signals. Consequently, much of the current knowledge on sexual selection is based directly or indirectly on human vision, which may or may not emphasize spectral information in a signal differently from the intended receiver. In an attempt to quantify this discrepancy, we used retinal models to test whether human and bird vision rank plumage colors similarly. Of 67 species, human and bird models disagreed in 26 as to which pair of patches in the plumage provides the strongest color contrast or which male in a random pair is the more colorful. These results were only partly attributable to human UV blindness. Despite confirming a strong correlation between avian and human color discrimination, we conclude that a significant proportion of the information in avian visual signals may be lost in translation.

Evolution of ultraviolet vision in shorebirds (Charadriiformes)

Diurnal birds belong to one of two classes of colour vision. These are distinguished by the maximum absorbance wavelengths of the SWS1 visual pigment sensitive to violet (VS) and ultraviolet (UVS). Shifts between the classes have been rare events during avian evolution. Gulls (Laridae) are the only shorebirds (Charadriiformes) previously reported to have the UVS type of opsin, but too few species have been sampled to infer that gulls are unique among shorebirds or that Laridae is monomorphic for this trait. We have sequenced the SWS1 opsin gene in a broader sample of species. We confirm that cysteine in the key amino acid position 90, characteristic of the UVS class, has been conserved throughout gull evolution but also that the terns Anous minutus, A. tenuirostris and Gygis alba, and the skimmer Rynchops niger carry this trait. Terns, excluding Anous and Gygis, share the VS conferring serine in position 90 with other shorebirds but it is translated from a codon more similar to that found in UVS shorebirds. The most parsimonious interpretation of these findings, based on a molecular gene tree, is a single VS to UVS shift and a subsequent reversal in one lineage.

The presence of UV wavelengths improves the temporal resolution of the avian visual system

SUMMARY The ability to perceive rapid movement is an essential adaptation in birds, which are involved in rapid flight, pursuing prey and escaping predators. Nevertheless, the temporal resolution of the avian visual systems has been less well explored than spectral sensitivity. There are indications that birds are superior to humans in their ability to detect movement, as suggested by higher critical flicker frequencies (CFFs). It has also been implied, but not properly tested, that properties of CFF, as a function of light intensity, are affected by the spectral composition of light. This study measured CFF in the chicken, Gallus gallus L., using four different light stimuli – white, full-spectrum (white with addition of UV), yellow (590 nm) and UV (400 nm) – and four light intensity levels, adjusted to relative cone sensitivity. The results showed significantly higher CFF values for full-spectrum compared with white light, as well as a steeper rate of increase with intensity. The presence of UV wavelengths, previously demonstrated to affect mate choice and foraging, appears to be important also for detection of rapid movement. The yellow and UV light stimuli yielded rather similar CFFs, indicating no special role for the double cone in flicker detection.

Cranial neural crest-cell migration in the direct-developing frog, Eleutherodactylus coqui: molecular heterogeneity within and among migratory streams

Direct development is a specialized reproductive mode that has evolved repeatedly in many different lineages of amphibians, especially anurans. A fully formed, albeit miniature adult hatches directly from the egg; there is no free-living larva. In many groups, the evolution of direct development has had profound consequences for cranial development and morphology, including many components that are derived from the embryonic neural crest. Yet, the developmental bases of these effects remain poorly known. In order to more fully characterize these changes, we used three molecular markers to analyze cranial neural crest-cell emergence and migration in the direct-developing frog, Eleutherodactylus coqui: HNK-1 immunoreactivity, Dlx protein expression, and cholinesterase activity. Our study validates and extends earlier results showing that the comprehensive changes in embryonic cranial patterning, differentiation, and developmental timing that are associated with direct development in Eleutherodactylus have not affected gross features of cranial neural crest biology: the relative timing of crest emergence and the number, configuration and identity of the principal migratory streams closely resemble those seen in metamorphic anurans. The three markers are variably expressed within and among neural crest-cell populations. This variation suggests that determination of cranial neural crest-cells may already have begun at or soon after the onset of migration, when the cells emerge from the neural tube. It is not known how or even if this variation correlates with differential cell lineage or fate. Finally, although HNK-1 expression is widely used to study neural crest migration in teleost fishes and amniotes, E. coqui is the only amphibian known in which it effectively labels migrating neural crest-cells. There are not enough comparative data to determine whether this feature is functionally associated with direct development or is instead unrelated to reproductive mode.