Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments

The violet- and ultraviolet-sensitive visual pigments of birds belong to the same class of pigments as the violet-sensitive (so-called blue) pigments of mammals. However, unlike the pigments from mammals and other vertebrate taxa which, depending on species, have lambda(max) values of either around 430 nm or around 370 nm, avian pigments are found with lambda(max) values spread across this range. In this paper, we present the sequences of two pigments isolated from Humbolt penguin and pigeon with intermediate lambda(max) values of 403 and 409 nm, respectively. By comparing the amino acid sequences of these pigments with the true UV pigments of budgerigar and canary and with chicken violet with a lambda(max) value of 420 nm, we have been able to identify five amino acid sites that show a pattern of substitution between species that is consistent with differences in lambda(max). Each of these substitutions has been introduced into budgerigar cDNA and expressed in vitro in COS-7 cells. Only three resulted in spectral shifts in the regenerated pigment; two had relatively small effects and may account for the spectral shifts between penguin, pigeon, and chicken whereas one, the replacement of Ser by Cys at site 90 in the UV pigments, produced a 35 nm shortwave shift that could account for the spectral shift from 403 nm in penguin to around 370 nm in budgerigar and canary.     

Spectral tuning and evolution of primate short-wavelength-sensitive visual pigments

The peak sensitivities (λ(max)) of the short-wavelength-sensitive-1 (SWS1) pigments in mammals range from the ultraviolet (UV) (360-400 nm) to the violet (400-450 nm) regions of the spectrum. In most cases, a UV or violet peak is determined by the residue present at site 86, with Phe conferring UV sensitivity (UVS) and either Ser, Tyr or Val causing a shift to violet wavelengths. In primates, however, the tuning mechanism of violet-sensitive (VS) pigments would appear to differ. In this study, we examine the tuning mechanisms of prosimian SWS1 pigments. One species, the aye-aye, possesses a pigment with Phe86 but in vitro spectral analysis reveals a VS rather than a UVS pigment. Other residues (Cys, Ser and Val) at site 86 in prosimians also gave VS pigments. Substitution at site 86 is not, therefore, the primary mechanism for the tuning of VS pigments in primates, and phylogenetic analysis indicates that substitutions at site 86 have occurred at least five times in primate evolution. The sole potential tuning site that is conserved in all primate VS pigments is Pro93, which when substituted by Thr (as found in mammalian UVS pigments) in the aye-aye pigment shifted the peak absorbance into the UV region with a λ(max) value at 371 nm. We, therefore, conclude that the tuning of VS pigments in primates depends on Pro93, not Tyr86 as in other mammals. However, it remains uncertain whether the initial event that gave rise to the VS pigment in the ancestral primate was achieved by a Thr93Pro or a Phe86Tyr substitution.     

Wavelength modulation by molecular environment in visual pigments

The absorption and regenerability characteristics are compared for rhodopsin contained in rod outer segment membranes and purified in a series of alkyl sucrose esters. It is found that membrane-bound rhodopsin has maximum absorbance from 504 to 500 nm between 1.5 and 40 degrees C. After purification, rhodopsin absorbance can be blue-shifted by up to 6 nm, depending on the detergent species used. Only the longest chain sucrose esters give purified rhodopsin with maximum absorbance comparable to that of the native pigment. In the same manner, detergent-purified rhodopsin will be easily regenerated as long as its native spectral characteristics are maintained. Sucrose esters thus prove to be mild enough to maintain rhodopsin functionality with respect to these two properties and could probably be used successfully to maintain other membrane proteins' integrity.     

Molecular characterization of crustacean visual pigments and the evolution of pancrustacean opsins

Investigations of opsin evolution outside of vertebrate systems have long been focused on insect visual pigments, whereas other groups have received little attention. Furthermore, few studies have explicitly investigated the selective influences across all the currently characterized arthropod opsins. In this study, we contribute to the knowledge of crustacean opsins by sequencing 1 opsin gene each from 6 previously uncharacterized crustacean species (Euphausia superba, Homarus gammarus, Archaeomysis grebnitzkii, Holmesimysis costata, Mysis diluviana, and Neomysis americana). Visual pigment spectral absorbances were measured using microspectrophotometry for species not previously characterized (A. grebnitzkii=496 nm, H. costata=512 nm, M. diluviana=501 nm, and N. americana=520 nm). These novel crustacean opsin sequences were included in a phylogenetic analysis with previously characterized arthropod opsin sequences to determine the evolutionary placement relative to the well-established insect spectral clades (long-/middle-/short-wavelength sensitive). Phylogenetic analyses indicate these novel crustacean opsins form a monophyletic clade with previously characterized crayfish opsin sequences and form a sister group to insect middle-/long-wavelength-sensitive opsins. The reconstructed opsin phylogeny and the corresponding spectral data for each sequence were used to investigate selective influences within arthropod, and mainly "pancrustacean," opsin evolution using standard dN/dS ratio methods and more sensitive techniques investigating the amino acid property changes resulting from nonsynonymous replacements in a historical (i.e., phylogenetic) context. Although the conservative dN/dS methods did not detect any selection, 4 amino acid properties (coil tendencies, compressibility, power to be at the middle of an alpha-helix, and refractive index) were found to be influenced by destabilizing positive selection. Ten amino acid sites relating to these properties were found to face the binding pocket, within 4 A of the chromophore and thus have the potential to affect spectral tuning.     

Gene duplications and evolution of the short wavelength-sensitive visual pigments in vertebrates

When invertebrate rhodopsins were used as the outgroup, the rootedphylogenetic tree of 26 vertebrate visual pigments (VPs) was constructed.These VPs are distinguished into the following four clusters: (1) RH1cluster consisting of rhodopsins, (2) RH2 cluster consisting of VPs withvariable ranges of absorption spectra, (3) SWS cluster of shortwavelength-sensitive VPs, and (4) LWS/MSW cluster of long and mediumwavelength-sensitive VPs. Short wavelength-sensitive VPs from Astyanaxfasciatus (AF23), goldfish (BCa), chicken (BCg and VGg), and human (BHs)belong to SWS cluster, whereas that from gecko (BGge) belongs to the RH2cluster. The SWS cluster is further divided into SWS-I (BHs and VGg) andSWS-II (AF23, BCa, and BGg) groups. The SWS-I group has accumulated moreamino acid changes than any other group of VPs. It is suggested that aminoacid changes at a few key positions might have been important in thefunctional differentiation of the SWS-I group from the SWS-II group.     

The evolution of the avian genome as revealed by comparative molecular cytogenetics

Birds are characterised by feathers, flight, a small genome and a very distinctive karyotype. Despite the large numbers of chromosomes, the diploid count of 2n approximately 80 has remained remarkably constant with 63% of birds where 2n = 74-86, 24% with 2n = 66-74 and extremes of 2n = 40 and 2n = 142. Of these, the most studied is the chicken (2n = 78), and molecular cytogenetic probes generated from this species have been used to further understand the evolution of the avian genome. The ancestral karyotype is, it appears, very similar to that of the chicken, with chicken chromosomes 1, 2, 3, 4q, 5, 6, 7, 8, 9, 4p and Z representing the ancestral avian chromosomes 1-10 + Z; chromosome 4 being the most ancient. Avian evolution occurred primarily in three stages: the divergence of the group represented by extant ratites (emu, ostrich etc.) from the rest; divergence of the Galloanserae (chicken, turkey, duck, goose etc.)--the most studied group; and divergence of the 'land' and 'water' higher birds. Other than sex chromosome differentiation in the first divergence there are no specific changes associated with any of these evolutionary milestones although certain families and orders have undergone multiple fusions (and some fissions), which has reduced their chromosome number; the Falconiformes are the best described. Most changes, overall, seem to involve chromosomes 1, 2, 4, 10 and Z where the Z changes are intrachromosomal; there are also some recurring (convergent) events. Of these, the most puzzling involves chromosomes 4 and 10, which appear to have undergone multiple fissions and/or fusions throughout evolution - three possible hypotheses are presented to explain the findings. We conclude by speculating as to the reasons for the strange behaviour of these chromosomes as well as the role of telomeres and nuclear organisation in avian evolution.     

The cone photoreceptors and visual pigments of chameleons

Visual pigments, oil droplets and photoreceptor types in the retinas of four species of true chameleons have been examined by microspectrophotometry. The species occupy different photic environments: two species of Chamaeleo are from Madagascar and two species of Furcifer are from Africa and the Arabian Peninsula. In addition to double cones, four spectrally distinct classes of single cone were identified. No rod photoreceptors were observed. The visual pigments appear to be mixtures of rhodopsins and porphyropsins. Double cones contained a pale oil droplet in the principle member and both outer segments contained a long-wave-sensitive visual pigment with a spectral maximum between about 555 nm and 610 nm, depending on the rhodopsin/porphyropsin mixture. Long-wave-sensitive single cones contained a visual pigment spectrally identical to the double cones, but combined with a yellow oil droplet. The other three classes of single cone contained visual pigments with maxima at about 480–505, 440–450 and 375–385 nm, combined with yellow, clear and transparent oil droplets respectively. The latter two classes were sparsely distributed. The transmission of the lens and cornea of C. dilepis was measured and found to be transparent throughout the visible and near ultraviolet, with a cut off at about 350 nm.     

Cone visual pigments

Cone visual pigments are visual opsins that are present in vertebrate cone photoreceptor cells and act as photoreceptor molecules responsible for photopic vision. Like the rod visual pigment rhodopsin, which is responsible for scotopic vision, cone visual pigments contain the chromophore 11-cis-retinal, which undergoes cis–trans isomerization resulting in the induction of conformational changes of the protein moiety to form a G protein-activating state. There are multiple types of cone visual pigments with different absorption maxima, which are the molecular basis of color discrimination in animals. Cone visual pigments form a phylogenetic sister group with non-visual opsin groups such as pinopsin, VA opsin, parapinopsin and parietopsin groups. Cone visual pigments diverged into four groups with different absorption maxima, and the rhodopsin group diverged from one of the four groups of cone visual pigments. The photochemical behavior of cone visual pigments is similar to that of pinopsin but considerably different from those of other non-visual opsins. G protein activation efficiency of cone visual pigments is also comparable to that of pinopsin but higher than that of the other non-visual opsins. Recent measurements with sufficient time-resolution demonstrated that G protein activation efficiency of cone visual pigments is lower than that of rhodopsin, which is one of the molecular bases for the lower amplification of cones compared to rods. In this review, the uniqueness of cone visual pigments is shown by comparison of their molecular properties with those of non-visual opsins and rhodopsin. This article is part of a Special Issue entitled: Retinal Proteins — You can teach an old dog new tricks.     

Molecular characterization of visual pigments in Branchiopoda and the evolution of opsins in Arthropoda

Studies on color vision in invertebrates have focused primarily on insect visual pigments, with little attention given to crustacean visual pigments. None of the blue-green-, blue-, or ultraviolet (UV)-sensitive-opsins have been identified in crustaceans. In addition, the discussion of visual pigments has been limited to long-wavelength-sensitive opsins in Pancrustacea. Here, we focused on Branchiopoda (Crustacea), which is a sister group of Hexapoda including insects. In the tadpole shrimp Triops granarius, the visual pigment chromophore was retinal. Multiple opsins were isolated from each of three branchiopod species, T. granarius, Triops longicaudatus, and the fairy shrimp Branchinella kugenumaensis (five, five, and four opsins from these species, respectively). Phylogenetic analyses and the presence of a lysine residue corresponding to position 90 in bovine rhodopsin suggested that three of the branchiopod opsins comprise UV-sensitive pigments. In addition, the phylogenetic relationships between insect and branchiopod UV-sensitive opsins revealed that the divergence of blue- and UV-sensitive pigments predates the Branchiopoda and Insecta divergence. The other branchiopod opsins show distant relationships to other known insect opsins and form novel clusters. The present results strongly suggest that the ancestral arthropod of the Chelicerata-Pancrustacea lineages possessed at least four types of opsins. The ancestors of Pancrustacea and the Insecta-Branchiopoda lineages possessed at least five and six types of opsins, respectively. Our results suggest that in the evolutionary process associated with each lineage, several opsins appeared and diversified with repeated gene duplication, of which some have been lost in some taxa.     

Three fundamental contributions of molecular genetics to avian ecology and evolution

Studies in molecular genetics are having revisionary impact in at least three broad areas of avian ecology and evolution: mating systems, geographic population structure and gene flow, and phylogenetic relationships among species and higher taxa. With regard to mating systems, genetic analyses of maternity and paternity have revealed unexpectedly high frequencies of extra-pair fertilization and intraspecific brood parasitism in numerous avian species (including those thought to be socially monogamous), and these discoveries are prompting a fundamental reshaping of mating system theory for birds. With regard to genetic structure, molecular markers have uncovered a great variety of depths and patterns in the phylogeographic histories of conspecific populations, and these findings provide novel perspectives on historical gene flow regimes and species concepts. With regard to evolutionary relationships among higher avian taxa, molecular findings have suggested several phylogenetic realignments, thus prompting renewed interest in the cross-comparative aspects of molecular and morphological evolution as well as of alternative procedures for molecular analysis.     

Three fundamental contributions of molecular genetics to avian ecology and evolution

Studies in molecular genetics are having revisionary impact in at least three broad areas of avian ecology and evolution: mating systems, geographic population structure and gene flow, and phylogenetic relationships among species and higher taxa. With regard to mating systems, genetic analyses of maternity and paternity have revealed unexpectedly high frequencies of extra-pair fertilization and intraspecific brood parasitism in numerous avian species (including those thought to be socially monogamous), and these discoveries are prompting a fundamental reshaping of mating system theory for birds. With regard to genetic structure, molecular markers have uncovered a great variety of depths and patterns in the phylogeographic histories of conspecific populations, and these findings provide novel perspectives on historical gene flow regimes and species concepts. With regard to evolutionary relationships among higher avian taxa, molecular findings have suggested several phylogenetic realignments, thus prompting renewed interest in the cross-comparative aspects of molecular and morphological evolution as well as of alternative procedures for molecular analysis.     

Fly visual pigments difference in visual pigments of blowfly and dronefly peripheral retinula cells

Journal of Comparative Physiology A - The visual pigments of peripheral retinula cells in fly eyes have been investigated by microspectrophotometry in vivo. Since flies have a pupil mechanism...     

The visual pigments of four deep-sea crustacean species

Summary The visual pigments of four mesopelagic crustacean species were studied at sea by means of microspectrophotometry. The absorbance maxima obtained for the visual pigments and their metarhodopsins, respectively, were: 493 nm and 481 nm (Systellaspis debilis), 485 nm and 480 nm (Acanthephyra curtirostris), 491 nm and 482 nm (A. smithi), and 495 nm and 487 nm (Sergestes tenuiremis). The spectral characteristics of the rhodopsins and metarhodopsins permit high photosensitivity and facilitate photoregeneration in a nearly monochromatic environment. Photic regeneration of rhodopsins from the deep-sea environment was demonstrated, and data were obtained which are consistent with the occurrence of dark regeneration. Specific optical density of the observed visual pigments was calculated for two species.     

The gecko visual pigments. The behavior of opsin

The 521-pigment extracted out of the retina of the Tokay gecko has the typical stereospecificity of the vertebrate visual pigments. This is true for the pigment in the chloride-depleted, "blue-shifted" state as well as for the normal pigment with added chloride. While in the chloride-deficient state, pigment regeneration occurred with both 11-cis- and 9-cis-retinals and the regenerated photopigments were also in the blue-shifted, chloride-depleted state. As with the native pigment, these regenerated pigments were bathochromically shifted to their normal positions by the addition of chloride. Chloride-deficient opsin by itself also responded to chloride for the pigment regenerated with 11-cis-retinal from such chloride-treated opsin was in the normal 521-position. Regeneration was always rapid, reaching completion in less than 5 min, and was significantly faster than for cow rhodopsin regenerating under the same conditions. This rapid rate was found with or without chloride, with both 11-cis- and 9-cis-retinals and in the presence of the sulfhydryl poison, p-hydroxymercuribenzoate (PMB). Like the native chloride-deficient pigment, the regenerated chloride-depleted photopigments responded to PMB by a blue shift beyond the position of the chloride-deficient state. The addition of chloride to these "poisoned" regenerated pigments caused a bathochromic shift of such magnitude as to indicate a repair of both the PMB and chloride-deficient blue shift. In this discussion the possible implications of these results to phylogenetic considerations are considered as well as to some molecular properties of the 521-pigment.     

The evolution of avian parental care

A stage model traces key behavioural tactics and life-history traits that are involved in the transition from promiscuity with no parental care, the mating system that typifies reptiles, to that typical of most birds, social monogamy with biparental care. In stage I, females assumed increasing parental investment in precocial young, female choice of mates increased, female-biased mating dispersal evolved and population sex ratios became male biased. In stage II, consortships between mating partners allowed males to attract rare social mates, provided a mechanism for paternity assessment and increased female ability to assess mate quality. In stage III, relative female scarcity enabled females to demand parental investment contributions from males having some paternity certainty. This innovation was facilitated by the nature of avian parental care; i.e. most care-giving activities can be adopted in small units. Moreover, the initial cost of care giving to males was small compared with its benefit to females. Males, however, tended to decline to assume non-partitionable, risky, or relatively costly parental activities. In stage IV, altriciality coevolved with increasing biparental care, resulting in social monogamy. Approaches for testing behavioural hypotheses are suggested.