Photochemical nature of parietopsin

Parietopsin is a nonvisual green light-sensitive opsin closely related to vertebrate visual opsins and was originally identified in lizard parietal eye photoreceptor cells. To obtain insight into the functional diversity of opsins, we investigated by UV-visible absorption spectroscopy the molecular properties of parietopsin and its mutants exogenously expressed in cultured cells and compared the properties to those of vertebrate and invertebrate visual opsins. Our mutational analysis revealed that the counterion in parietopsin is the glutamic acid (Glu) in the second extracellular loop, corresponding to Glu181 in bovine rhodopsin. This arrangement is characteristic of invertebrate rather than vertebrate visual opsins. The photosensitivity and the molar extinction coefficient of parietopsin were also lower than those of vertebrate visual opsins, features likewise characteristic of invertebrate visual opsins. On the other hand, irradiation of parietopsin yielded meta-I, meta-II, and meta-III intermediates after batho and lumi intermediates, similar to vertebrate visual opsins. The pH-dependent equilibrium profile between meta-I and meta-II intermediates was, however, similar to that between acid and alkaline metarhodopsins in invertebrate visual opsins. Thus, parietopsin behaves as an "evolutionary intermediate" between invertebrate and vertebrate visual opsins.     

The putative brain photoperiodic photoreceptors in the vetch aphid,Megoura viciae

In an attempt to identify the brain photoreceptors that mediate the photoperiodic response of the vetch aphid, Megoura viciae, we utilised immunocytochemical techniques and employed 20 antibodies directed against invertebrate and vertebrate opsins and phototransduction proteins. A sub-set of these antibodies (to Drosophila rhodopsin 1: RH1-1; vertebrate cone opsins: COS-1; CERN-874; CERN-933; vertebrate rod opsin: CERN-901; vertebrate arrestin: AB-Arr; vertebrate transducin+arrestin+rhodopsin kinase+cGMP phosphodiesterase: CERN-911; and vertebrate cellular retinoid binding protein: CRALBP) consistently labelled an anterior ventral neuropile region of the protocerebrum. These anatomical findings, coupled with previous localised illumination and micro-lesion studies, provide strong evidence that this region of the aphid brain houses the photoperiodic photoreceptors. The present study also confirms that the medial (Group I) neurosecretory cells are not the photoperiodic photoreceptors.     

Evolution and functional diversity of jellyfish opsins

Cnidaria are the most basal animal phylum possessing complex eyes [1]. Their eyes predominantly use ciliary photoreceptor cells (c-PRCs) like vertebrates, whereas insect eyes use rhabdomeric photoreceptor cells (r-PRCs) [1-4]. These two cell types show not only different cytoarchitectures but distinct phototransduction cascades, which are triggered by the respective types of opsins (e.g., [5]), ciliary opsins (c-opsins) and rhabdomeric opsins (r-opsins) [6]. Recent reports suggested that the c- and r-PRCs and their respective opsins diverged at least before the deuterostome-protostome split [7-9]. To study the earlier evolution of animal PRCs and opsins, we investigated two hydrozoan jellyfishes. We report here the first-characterized cnidarian opsins. Molecular phylogeny revealed that the cloned 20 jellyfish opsins, together with all the opsins from a hydra and some from a sea anemone, are more closely related to the c-opsins than to any other major opsin subfamily, indicating that the divergence of c- and r-opsins antedates the Cnidaria-Bilateria split. Possible scenarios of animal PRC evolution are discussed. Furthermore, Cladonema opsins show several distinct tissue- and stage-specific expression patterns. The expression of specific opsins in the eyes suggests a role in vision, whereas that in the gonads suggests a role in light-controlled release of gametes.     

UV photoreceptors and UV-yellow wing pigments in Heliconius butterflies allow a color signal to serve both mimicry and intraspecific communication

Mimetic wing coloration evolves in butterflies in the context of predator confusion. Unless butterfly eyes have adaptations for discriminating mimetic color variation, mimicry also carries a risk of confusion for the butterflies themselves. Heliconius butterfly eyes, which express recently duplicated ultraviolet (UV) opsins, have such an adaptation. To examine bird and butterfly color vision as sources of selection on butterfly coloration, we studied yellow wing pigmentation in the tribe Heliconiini. We confirmed, using reflectance and mass spectrometry, that only Heliconius use 3-hydroxy-DL-kynurenine (3-OHK), which looks yellow to humans but reflects both UV- and long-wavelength light, whereas butterflies in related genera have chemically unknown yellow pigments mostly lacking UV reflectance. Modeling of these color signals reveals that the two UV photoreceptors of Heliconius are better suited to separating 3-OHK from non-3-OHK spectra compared with the photoreceptors of related genera or birds. The co-occurrence of potentially enhanced UV vision and a UV-reflecting yellow wing pigment could allow unpalatable Heliconius private intraspecific communication in the presence of mimics. Our results are the best available evidence for the correlated evolution of a color signal and color vision. They also suggest that predator visual systems are error prone in the context of mimicry.     

Molecular Evolution of Arthropod Color Vision Deduced from Multiple Opsin Genes of Jumping Spiders

Among terrestrial animals, only vertebrates and arthropods possess wavelength-discrimination ability, so-called “color vision”. For color vision to exist, multiple opsins which encode visual pigments sensitive to different wavelengths of light are required. While the molecular evolution of opsins in vertebrates has been well investigated, that in arthropods remains to be elucidated. This is mainly due to poor information about the opsin genes of non-insect arthropods. To obtain an overview of the evolution of color vision in Arthropoda, we isolated three kinds of opsins, Rh1, Rh2, and Rh3, from two jumping spider species, Hasarius adansoni and Plexippus paykulli. These spiders belong to Chelicerata, one of the most distant groups from Hexapoda (insects), and have color vision as do insects. Phylogenetic analyses of jumping spider opsins revealed a birth and death process of color vision evolution in the arthropod lineage. Phylogenetic positions of jumping spider opsins revealed that at least three opsins had already existed before the Chelicerata-Pancrustacea split. In addition, sequence comparison between jumping spider Rh3 and the shorter wavelength-sensitive opsins of insects predicted that an opsin of the ancestral arthropod had the lysine residue responsible for UV sensitivity. These results strongly suggest that the ancestral arthropod had at least trichromatic vision with a UV pigment and two visible pigments. Thereafter, in each pancrustacean and chelicerate lineage, the opsin repertoire was reconstructed by gene losses, gene duplications, and function-altering amino acid substitutions, leading to evolution of color vision. Mitsumasa Koyanagi and Takashi Nagata contributed equally to this work. Sequence data from this article have been deposited with the DDBJ under accession nos. AB251846–AB251851.     

Opsin evolution and expression in Arthropod compound Eyes and Ocelli: Insights from the cricket Gryllus bimaculatus

ABSTRACT: BACKGROUND: Opsins are key proteins in animal photoreception. Together with a light-sensitive group, the chromophore, they form visual pigments which initiate the visual transduction cascade when photoactivated. The spectral absorption properties of visual pigments are mainly determined by their opsins, and thus opsins are crucial to understand the adaptations of animal eyes. Studies on the phylogeny and expression pattern of opsins have received considerable attention, but our knowledge about insect visual opsins is still limited. Up to now, researchers have focused on holometabolous insects, while general conclusions require sampling from a broader range of taxa. We have therefore investigated visual opsins in the ocelli and compound eyes of the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect. RESULTS: Phylogenetic analyses place all identified cricket sequences within the three main visual opsin clades of insects. We assign three of these opsins to visual pigments found in the compound eyes with peak absorbances in the green (515 nm), blue (445 nm) and UV (332 nm) spectral range. Their expression pattern divides the retina into distinct regions: (1) the polarization-sensitive dorsal rim area with blue- and UV-opsin, (2) a newly-discovered ventral band of ommatidia with blue- and green-opsin and (3) the remainder of the compound eye with UV- and green-opsin. In addition, we provide evidence for two ocellar photopigments with peak absorbances in the green (511 nm) and UV (350 nm) spectral range, and with opsins that differ from those expressed in the compound eyes. CONCLUSIONS: Our data show that cricket eyes are spectrally more specialized than has previously been assumed, suggesting that similar adaptations in other insect species might have been overlooked. The arrangement of spectral receptor types within some ommatidia of the cricket compound eyes differs from the generally accepted pattern found in holometabolous insect taxa and awaits a functional explanation. From the opsin phylogeny, we conclude that gene duplications, which permitted differential opsin expression in insect ocelli and compound eyes, occurred independently in several insect lineages and are recent compared to the origin of the eyes themselves.     

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.     

Activation of Transducin by Bistable Pigment Parapinopsin in the Pineal Organ of Lower Vertebrates

Pineal organs of lower vertebrates contain several kinds of photosensitive molecules, opsins that are suggested to be involved in different light-regulated physiological functions. We previously reported that parapinopsin is an ultraviolet (UV)-sensitive opsin that underlies hyperpolarization of the pineal photoreceptor cells of lower vertebrates to achieve pineal wavelength discrimination. Although, parapinopsin is phylogenetically close to vertebrate visual opsins, it exhibits a property similar to invertebrate visual opsins and melanopsin: the photoproduct of parapinopsin is stable and reverts to the original dark states, demonstrating the nature of bistable pigments. Therefore, it is of evolutionary interest to identify a phototransduction cascade driven by parapinopsin and to compare it with that in vertebrate visual cells. Here, we showed that parapinopsin is coupled to vertebrate visual G protein transducin in the pufferfish, zebrafish, and lamprey pineal organs. Biochemical analyses demonstrated that parapinopsins activated transducin in vitro in a light-dependent manner, similar to vertebrate visual opsins. Interestingly, transducin activation by parapinopsin was provoked and terminated by UV- and subsequent orange-lights irradiations, respectively, due to the bistable nature of parapinopsin, which could contribute to a wavelength-dependent control of a second messenger level in the cell as a unique optogenetic tool. Immunohistochemical examination revealed that parapinopsin was colocalized with Gt2 in the teleost, which possesses rod and cone types of transducin, Gt1, and Gt2. On the other hand, in the lamprey, which does not possess the Gt2 gene, in situ hybridization suggested that parapinopsin-expressing photoreceptor cells contained Gt1 type transducin GtS, indicating that lamprey parapinopsin may use GtS in place of Gt2. Because it is widely accepted that vertebrate visual opsins having a bleaching nature have evolved from non-bleaching opsins similar to parapinopsin, these results implied that ancestral bistable opsins might acquire coupling to the transducin-mediated cascade and achieve light-dependent hyperpolarizing response of the photoreceptor cells.     

Vertebrate ancient-long opsin has molecular properties intermediate between those of vertebrate and invertebrate visual pigments

VA/VAL opsin is one of the four kinds of nonvisual opsins that are closely related to vertebrate visual pigments in the phylogenetic tree of opsins. Previous studies indicated that among these opsins, parapinopsin and pinopsin exhibit molecular properties similar to those of invertebrate bistable visual pigments and vertebrate visual pigments, respectively. Here we show that VA/VAL opsin exhibits molecular properties intermediate between those of parapinopsin and pinopsin. VAL opsin from Xenopus tropicalis was expressed in cultured cells, and the pigment with an absorption maximum at 501 nm was reconstituted by incubation with 11-cis-retinal. Light irradiation of this pigment caused cis-to-trans isomerization of the chromophore to form a state having an absorption maximum in the visible region. This state has the ability to activate Gi and Gt types of G proteins. Therefore, the active state of VAL opsin is a visible light-absorbing intermediate, which probably has a protonated retinylidene Schiff base as its chromophore, like the active state of parapinopsin. However, this state was apparently photoinsensitive and did not show reverse reaction to the original pigment, unlike the active state of parapinopsin, and instead similar to that of pinopsin. Furthermore, the Gi activation efficiency of VAL opsin was between those of pinopsin and parapinopsin. Thus, the molecular properties of VA/VAL opsin give insights into the mechanism of conversion of the molecular properties from invertebrate to vertebrate visual pigments.     

Color vision diversity and significance in primates inferred from genetic and field studies

Color provides a reliable cue for object detection and identification during various behaviors such as foraging, mate choice, predator avoidance and navigation. The total number of colors that a visual system can discriminate is largely dependent on the number of different spectral types of cone opsins present in the retina and the spectral separations among them. Thus, opsins provide an excellent model system to study evolutionary interconnections at the genetic, phenotypic and behavioral levels. Primates have evolved a unique ability for three-dimensional color vision (trichromacy) from the two-dimensional color vision (dichromacy) present in the majority of other mammals. This was accomplished via allelic differentiation (e.g. most New World monkeys) or gene duplication (e.g. Old World primates) of the middle to long-wavelength sensitive (M/LWS, or red–green) opsin gene. However, questions remain regarding the behavioral adaptations of primate trichromacy. Allelic differentiation of the M/LWS opsins results in extensive color vision variability in New World monkeys, where trichromats and dichromats are found in the same breeding population, enabling us to directly compare visual performances among different color vision phenotypes. Thus, New World monkeys can serve as an excellent model to understand and evaluate the adaptive significance of primate trichromacy in a behavioral context. I shall summarize recent findings on color vision evolution in primates and introduce our genetic and behavioral study of vision-behavior interrelationships in free-ranging sympatric capuchin and spider monkey populations in Costa Rica.     

Diversity of Active States in TMT Opsins

Opn3/TMT opsins belong to one of the opsin groups with vertebrate visual and non-visual opsins, and are widely distributed in eyes, brains and other internal organs in various vertebrates and invertebrates. Vertebrate Opn3/TMT opsins are further classified into four groups on the basis of their amino acid identities. However, there is limited information about molecular properties of these groups, due to the difficulty in preparing the recombinant proteins. Here, we successfully expressed recombinant proteins of TMT1 and TMT2 opsins of medaka fish (Oryzias latipes) in cultured cells and characterized their molecular properties. Spectroscopic and biochemical studies demonstrated that TMT1 and TMT2 opsins functioned as blue light-sensitive Gi/Go-coupled receptors, but exhibited spectral properties and photo-convertibility of the active state different from each other. TMT1 opsin forms a visible light-absorbing active state containing all-trans-retinal, which can be photo-converted to 7-cis- and 9-cis-retinal states in addition to the original 11-cis-retinal state. In contrast, the active state of TMT2 opsin is a UV light-absorbing state having all-trans-retinal and does not photo-convert to any other state, including the original 11-cis-retinal state. Thus, TMT opsins are diversified so as to form a different type of active state, which may be responsible for their different functions.     

Membrane and cellular properties in oscillating networks: implications for respiration

Because of a number of major advances in the past one to two decades, there is little doubt that the inherent cellular and membrane properties of neurons in an oscillating network play an important role in shaping the output of that network. There are a number of such examples in vertebrate and invertebrate systems. In this review, we present some of the newer methods that have been used in the identification of membrane properties and detail some cellular studies performed in both vertebrate (locomotion and sleep/waking rhythms) and invertebrate network systems (escape swimming in Tritonia diomedia and pyloric rhythm in Panulirus interruptus). Studies examining the cellular or membrane properties of respiratory neurons have been scarce until recently. The importance of these properties in dictating respiratory rhythm generation and output in the mature and immature animal is not yet known; however, we put this issue in perspective by building a parallel between mammalian respiration and other vertebrate networks that have been better investigated and characterized.     

Vertebrate/Invertebrate Trackways

The Ichnology Workshop held in 1998 in Bornholm, DK, evidenced significant differences between approaches used for studying vertebrate and invertebrate ichnites. In particular, trackways are used more in invertebrate ichno-studies than in vertebrate studies. This is due to the intrinsic characteristics of each category, primarily the multiple consequences of the order of magnitude gap in sizes, the opportunity to have more taxonomic information of the trackmaker with vertebrate ichnites, the usefulness of correlations with biotopes and facies with invertebrate ichnites, and practical parameters such as the probability of findings. That vertebrate and invertebrate ichnologists exchange ideas could certainly bring progress, however, significant differences between the two fields certainly remain. Using information on animal behavior to define ichnotaxobases would not be acceptable for most vertebrate tracks.     

Libbie Henrietta Hyman (1888-1969): from developmental mechanics to the evolution of animal body plans

Libbie Hyman is the most influential comparative invertebrate zoologist of the 20th century in the English-speaking world. During the first part of her career Hyman conducted experimental research on the metabolic and developmental physiology of a host of invertebrates and vertebrate embryos. One important aim of these studies was to elucidate the hidden processes of morphogenesis. Some of the papers from this early phase of Hyman's career already contain the seeds for her subsequent occupation with comparative embryology and morphology to address questions about animal body plan evolution and metazoan phylogeny. Hyman's views on invertebrate evolution and phylogeny have become widely incorporated into textbooks, and until very recently Hyman's ideas have been equated with 'traditional' or 'classical' views on animal evolution. Hyman's enduring fame and significance for modern evo-devo is primarily based upon her magisterial six-volume series The Invertebrates, which is the most encompassing single-author synthesis of invertebrate structure and development of the 20th century. In The Invertebrates Hyman addressed numerous questions about the evolution of animal body plans and metazoan phylogeny that are nowadays core items on the research agenda of evo-devo. In addition, Hyman had a lasting influence on teaching with the publication of her widely used laboratory manuals for elementary zoology, and especially comparative vertebrate anatomy.     

Optimization, constraint, and history in the evolution of eyes

Several features of the evolution of eyes and photoreceptors are examined in an effort to explore the relative roles of adaptation and historical and developmental constraints. Optical design shows clear evidence of adaptation, which in some respects approaches optima predictable from physics. The primate fovea, on the other hand, illustrates how adaptation can be channeled by developmental heritage. The primary structures of opsins reveal multiple evolutionary lineages within both Drosophila and humans. The pigments of vertebrae rods comprise a subset of opsins whose evolutionary relationships map onto the phylogeny of the parent species. The evolutionary reasons for why most rod pigments absorb maximally at 500 +/- 10 nm are obscure, as there is no convincing explanation based on adaptation alone. Rods are appropriately distinguished from cones on the basis of which opsin gene is expressed. This criterion is likely to be in conflict with other definitions in phyletic lines (e.g., geckos, snakes) that have long diurnal or nocturnal histories accompanied by loss of one or more opsin genes, followed by a secondary adaptation to life in a different photic environment. Color vision--a generalizable perception associated with the spectral composition of light--is usefully distinguished from wavelength-specific behaviors. The latter are also based on multiple visual pigments and more than one spectral class of receptors but cannot be altered by learning. The distinction is particularly forceful in bees, which exhibit both kinds of behavior. The evolution of primate color vision has been shaped by historical factors involving an extensive period of early mammalian nocturnality. Birds, by contrast, have more elaborate cones and a richer set of visual pigments. Avian color space can be represented in a tetrahedron.     

Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys?

Invertebrates are the main source of protein for many small-to-medium sized monkeys. Prey vary in size, mobility, degree of protective covering, and use of the forest, I.e. Canopy height, and whether they are exposed or embed themselves in substrates. Sex-differentiation in foraging patterns is well documented for some monkey species and recent studies find that color vision phenotype can also affect invertebrate foraging. Since vision phenotype is polymorphic and sex-linked in most New World monkeys - males have dichromatic vision and females have either dichromatic or trichromatic vision - this raises the possibility that sex differences are linked to visual ecology. We tested predicted sex differences for invertebrate foraging in white-faced capuchins Cebus capucinus and conducted 12 months of study on four free-ranging groups between January 2007 and September 2008. We found both sex and color vision effects. Sex: Males spent more time foraging for invertebrates on the ground. Females spent more time consuming embedded, colonial invertebrates, ate relatively more "soft" sedentary invertebrates, and devoted more of their activity budget to invertebrate foraging. Color Vision: Dichromatic monkeys had a higher capture efficiency of ex posed invertebrates and spent less time visually foraging. Trichromats ate relatively more "hard" sedentary invertebrates. We con clude that some variation in invertebrate foraging reflects differences between the sexes that may be due to disparities in size, strength, reproductive demands or niche preferences. However, other intraspecific variation in invertebrate foraging that might be mistakenly attributed to sex differences actually reflects differences in color vision.