Ultraviolet polarisation sensitivity in the stomatopod crustacean <Emphasis Type="Italic">Odontodactylus scyllarus</Emphasis>

The ommatidia of crustacean eyes typically contain two classes of photoreceptors with orthogonally oriented microvilli. These receptors provide the basis for two-channel polarisation vision in the blue–green spectrum. The retinae of gonodactyloid stomatopod crustaceans possess a great variety of structural specialisations for elaborate polarisation vision. One type of specialisation is found in the small, distally placed R8 cells within the two most ventral rows of the mid-band. These ultraviolet-sensitive photoreceptors produce parallel microvilli, a feature suggestive for polarisation-sensitive photoreceptors. Here, we show by means of intracellular recordings combined with dye-injections that in the gonodactyloid species Odontodactylus scyllarus, the R8 cells of mid-band rows 5 and 6 are sensitive to linear polarised ultraviolet light. We show that mid-band row 5 R8 cells respond maximally to light with an e-vector oriented parallel to the mid-band, whereas mid-band row 6 R8 cells respond maximally to light with an e-vector oriented perpendicular to the mid-band. This orthogonal arrangement of ultraviolet-sensitive receptor cells could support ultraviolet polarisation vision. R8 cells of rows 5 and 6 are known to act as quarter-wave retarders around 500 nm and thus are the first photoreceptor type described with a potential dual role in polarisation vision.     

Parallel processing and image analysis in the eyes of mantis shrimps

The compound eyes of mantis shrimps, a group of tropical marine crustaceans, incorporate principles of serial and parallel processing of visual information that may be applicable to artificial imaging systems. Their eyes include numerous specializations for analysis of the spectral and polarizational properties of light, and include more photoreceptor classes for analysis of ultraviolet light, color, and polarization than occur in any other known visual system. This is possible because receptors in different regions of the eye are anatomically diverse and incorporate unusual structural features, such as spectral filters, not seen in other compound eyes. Unlike eyes of most other animals, eyes of mantis shrimps must move to acquire some types of visual information and to integrate color and polarization with spatial vision. Information leaving the retina appears to be processed into numerous parallel data streams leading into the central nervous system, greatly reducing the analytical requirements at higher levels. Many of these unusual features of mantis shrimp vision may inspire new sensor designs for machine vision.     

Scanning eye movements of the stomatopod crustacean,Neogonodactylus oerstedii,in polarized light fields

ABSTRACT

Stomatopod crustaceans have highly mobile, independently moving compound eyes that are sensitive to both linearly and circularly polarized light. They rotate their eyes to predictable angles when viewing a linearly polarized target, and they scan their eyes frequently to sample the visual field. Angles of scans are roughly perpendicular to the plane of the midband (a set of specialized parallel rows of equatorial ommatidia). We investigated scanning eye movements in one Caribbean stomatopod species (Neogonodactylus oerstedii) in uniform visual fields that were vertically polarized, horizontally polarized, or depolarized. We found that mean eye rotation and scan angles differed significantly among these different treatments. Average scan angles differed by 12°, being more horizontal in a vertically polarized field than in a horizontally polarized one, and also more horizontal in a vertically polarized field than in a depolarized field. Thus, these stomatopods adjusted visual scanning to the polarization of the visual environment.     

Modelling the visual world of a velvet worm

In many animal phyla, eyes are small and provide only low-resolution vision for general orientation in the environment. Because these primitive eyes rarely have a defined image plane, traditional visual-optics principles cannot be applied. To assess the functional capacity of such eyes we have developed modelling principles based on ray tracing in 3D reconstructions of eye morphology, where refraction on the way to the photoreceptors and absorption in the photopigment are calculated incrementally for ray bundles from all angles within the visual field. From the ray tracing, we calculate the complete angular acceptance function of each photoreceptor in the eye, revealing the visual acuity for all parts of the visual field. We then use this information to generate visual filters that can be applied to high resolution images or videos to convert them to accurate representations of the spatial information seen by the animal. The method is here applied to the 0.1 mm eyes of the velvet worm Euperipatoides rowelli (Onychophora). These eyes of these terrestrial invertebrates consist of a curved cornea covering an irregular but optically homogeneous lens directly joining a retina packed with photoreceptive rhabdoms. 3D reconstruction from histological sections revealed an asymmetric eye, where the retina is deeper in the forward-pointing direction. The calculated visual acuity also reveals performance differences across the visual field, with a maximum acuity of about 0.11 cycles/deg in the forward direction despite laterally pointing eyes. The results agree with previous behavioural measurements of visual acuity, and suggest that velvet worm vision is adequate for orientation and positioning within the habitat.     

Photoreceptor projection and termination pattern in the lamina of gonodactyloid stomatopods (mantis shrimp)

The apposition compound eyes of gonodactyloid stomatopods are divided into a ventral and a dorsal hemisphere by six equatorial rows of enlarged ommatidia, the mid-band (MB). Whereas the hemispheres are specialized for spatial vision, the MB consists of four dorsal rows of ommatidia specialized for colour vision and two ventral rows specialized for polarization vision. The eight retinula cell axons (RCAs) from each ommatidium project retinotopically onto one corresponding lamina cartridge, so that the three retinal data streams (spatial, colour and polarization) remain anatomically separated. This study investigates whether the retinal specializations are reflected in differences in the RCA arrangement within the corresponding lamina cartridges. We have found that, in all three eye regions, the seven short visual fibres (svfs) formed by retinula cells 1–7 (R1–R7) terminate at two distinct lamina levels, geometrically separating the terminals of photoreceptors sensitive to either orthogonal e-vector directions or different wavelengths of light. This arrangement is required for the establishment of spectral and polarization opponency mechanisms. The long visual fibres (lvfs) of the eighth retinula cells (R8) pass through the lamina and project retinotopically to the distal medulla externa. Differences between the three eye regions exist in the packing of svf terminals and in the branching patterns of the lvfs within the lamina. We hypothesize that the R8 cells of MB rows 1–4 are incorporated into the colour vision system formed by R1–R7, whereas the R8 cells of MB rows 5 and 6 form a separate neural channel from R1 to R7 for polarization processing.This research was supported by the Swiss National Science Foundation (PBSKB-104268/1), the Australian Research Council (LP0214956) and the American Air Force (AOARD/AFOSR) (F62562-03-P-0227).     

Two visual systems in one eyestalk: The unusual optic lobe metamorphosis in the stomatopod Alima pacifica

The compound eyes of adult stomatopod crustaceans have two to six ommatidial rows at the equator, called the midband, that are often specialized for color and polarization vision. Beneath the retina, this midband specialization is represented as enlarged optic lobe lamina cartridges and a hernia‐like expansion in the medulla. We studied how the optic lobe transforms from the larvae, which possess typical crustacean larval compound eyes without a specialized midband, through metamorphosis into the adults with the midband in a two midband‐row species Alima pacifica. Using histological staining, immunolabeling, and 3D reconstruction, we show that the last‐stage stomatopod larvae possess double‐retina eyes, in which the developing adult visual system forms adjacent to, but separate from, the larval visual system. Beneath the two retinas, the optic lobe also contains two sets of optic neuropils, comprising of a larval lamina, medulla, and lobula, as well as an adult lamina, medulla, and lobula. The larval eye and all larval optic neuropils degenerate and disappear approximately a week after metamorphosis. In stomatopods, the unique adult visual system and all optic neuropils develop alongside the larval system in the eyestalk of last‐stage larvae, where two visual systems and two independent visual processing pathways coexist. © 2017 Wiley Periodicals, Inc. Develop Neurobiol 78: 3–14, 2018     

Reconstructing the eyes of Urbilateria

The shared roles of Pax6 and Six homologues in the eye development of various bilaterians suggest that Urbilateria, the common ancestors of all Bilateria, already possessed some simple form of eyes. Here, we re-address the homology of bilaterian cerebral eyes at the level of eye anatomy, of eye-constituting cell types and of phototransductory molecules. The most widespread eye type found in Bilateria are the larval pigment-cup eyes located to the left and right of the apical organ in primary, ciliary larvae of Protostomia and Deuterostomia. They can be as simple as comprising a single pigment cell and a single photoreceptor cell in inverse orientation. Another more elaborate type of cerebral pigment-cup eyes with an everse arrangement of photoreceptor cells is found in adult Protostomia. Both inverse larval and everse adult eyes employ rhabdomeric photoreceptor cells and thus differ from the chordate cerebral eyes with ciliary photoreceptors. This is highly significant because on the molecular level we find that for phototransduction rhabdomeric versus ciliary photoreceptor cells employ divergent rhodopsins and non-orthologous G-proteins, rhodopsin kinases and arrestins. Our comparison supports homology of cerebral eyes in Protostomia; it challenges, however, homology of chordate and non-chordate cerebral eyes that employ photoreceptor cells with non-orthologous phototransductory cascades.     

Determination of Photoreceptor Cell Spectral Sensitivity in an Insect Model from In Vivo Intracellular Recordings

Intracellular recording is a powerful technique used to determine how a single cell may respond to a given stimulus. In vision research, intracellular recording has historically been a common technique used to study sensitivities of individual photoreceptor cells to different light stimuli that is still being used today. However, there remains a dearth of detailed methodology in the literature for researchers wishing to replicate intracellular recording experiments in the eye. Here we present the insect as a model for examining eye physiology more generally. Insect photoreceptor cells are located near the surface of the eye and are therefore easy to reach, and many of the mechanisms involved in vision are conserved across animal phyla. We describe the basic procedure for in vivo intracellular recording of photoreceptor cells in the eye of a butterfly, with the goal of making this technique more accessible to researchers with little prior experience in electrophysiology. We introduce the basic equipment needed, how to prepare a live butterfly for recording, how to insert a glass microelectrode into a single cell, and finally the recording procedure itself. We also explain the basic analysis of raw response data for determining spectral sensitivity of individual cell types. Although our protocol focuses on determining spectral sensitivity, other stimuli (e.g., polarized light) and variations of the method are applicable to this setup.     

The agrin/perlecan-related protein eyes shut is essential for epithelial lumen formation in the Drosophila retina

The formation of epithelial lumina is a fundamental process in animal development. Each ommatidium of the Drosophila retina forms an epithelial lumen, the interrhabdomeral space, which has a critical function in vision as it optically isolates individual photoreceptor cells. Ommatidia containing an interrhabdomeral space have evolved from ancestral insect eyes that lack this lumen, as seen, for example, in bees. In a genetic screen, we identified eyes shut (eys) as a gene that is essential for the formation of matrix-filled interrhabdomeral space. Eys is closely related to the proteoglycans agrin and perlecan and secreted by photoreceptor cells into the interrhabdomeral space. The honeybee ortholog of eys is not expressed in photoreceptors, raising the possibility that recruitment of eys expression has made an important contribution to insect eye evolution. Our findings show that the secretion of a proteoglycan into the apical matrix is critical for the formation of epithelial lumina in the fly retina.     

Evolution of eye morphology and rhodopsin expression in the Drosophila melanogaster species subgroup

A striking diversity of compound eye size and shape has evolved among insects. The number of ommatidia and their size are major determinants of the visual sensitivity and acuity of the compound eye. Each ommatidium is composed of eight photoreceptor cells that facilitate the discrimination of different colours via the expression of various light sensitive Rhodopsin proteins. It follows that variation in eye size, shape, and opsin composition is likely to directly influence vision. We analyzed variation in these three traits in D. melanogaster, D. simulans and D. mauritiana. We show that D. mauritiana generally has larger eyes than its sibling species, which is due to a combination of larger ommatidia and more ommatidia. In addition, intra- and inter-specific differences in eye size among D. simulans and D. melanogaster strains are mainly caused by variation in ommatidia number. By applying a geometric morphometrics approach to assess whether the formation of larger eyes influences other parts of the head capsule, we found that an increase in eye size is associated with a reduction in the adjacent face cuticle. Our shape analysis also demonstrates that D. mauritiana eyes are specifically enlarged in the dorsal region. Intriguingly, this dorsal enlargement is associated with enhanced expression of rhodopsin 3 in D. mauritiana. In summary, our data suggests that the morphology and functional properties of the compound eyes vary considerably within and among these closely related Drosophila species and may be part of coordinated morphological changes affecting the head capsule.     

Vertebrate features revealed in the rudimentary eye of the Pacific hagfish (Eptatretus stoutii)

Hagfish eyes are markedly basic compared to the eyes of other vertebrates, lacking a pigmented epithelium, a lens and a retinal architecture built of three cell layers: the photoreceptors, interneurons and ganglion cells. Concomitant with hagfish belonging to the earliest-branching vertebrate group (the jawless Agnathans), this lack of derived characters has prompted competing interpretations that hagfish eyes represent either a transitional form in the early evolution of vertebrate vision, or a regression from a previously elaborate organ. Here, we show the hagfish retina is not extensively degenerating during its ontogeny, but instead grows throughout life via a recognizable PAX6+ ciliary marginal zone. The retina has a distinct layer of photoreceptor cells that appear to homogeneously express a single opsin of the RH1 rod opsin class. The epithelium that encompasses these photoreceptors is striking because it lacks the melanin pigment that is universally associated with animal vision; notwithstanding, we suggest this epithelium is a homologue of gnathosome retinal pigment epithelium (RPE) based on its robust expression of RPE65 and its engulfment of photoreceptor outer segments. We infer that the hagfish retina is not entirely rudimentary in its wiring, despite lacking a morphologically distinct layer of interneurons: multiple populations of cells exist in the hagfish inner retina and subsets of these express markers of vertebrate retinal interneurons. Overall, these data clarify Agnathan retinal homologies, reveal characters that now appear to be ubiquitous across the eyes of vertebrates, and refine interpretations of early vertebrate visual system evolution.     

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.     

Evolving eyes

Despite the incredible diversity among extant eyes, laws of physics constrain how light can be collected resulting in only eight known optical systems in animal eyes. Surprisingly, all animal eyes share a common molecular strategy using opsin for catching photons, but there are a diverse collection of mechanisms with proteins unrelated to each other used to focus light for vision. However, opsin is expressed in either one of two types of photoreceptor that differ fundamentally in their structure and tissue of origin. Taken together, this collection of observations strongly suggests that eyes have had multiple origins with remarkable convergence due to physics and molecular conservation of the opsin protein. Yet recent work has shown that a family of conserved genes are involved in eye formation despite substantial differences in their structure and origin, leading to a controversy over whether eyes evolved once or repeatedly. A likely resolution of this discussion is that particular genes and genetic programs have become associated with specific features needed for eyes and such suites of genes have been recruited as new eyes evolve. Since specific genes and their products are used repeatedly, it is somewhat difficult to conceptualize their causal relationships relative to evolutionary processes. However, detailed comparison of developmental programs may offer clues about multiple origins.     

Spectral tuning and the visual ecology of mantis shrimps

The compound eyes of mantis shrimps (stomatopod crustaceans) include an unparalleled diversity of visual pigments and spectral receptor classes in retinas of each species. We compared the visual pigment and spectral receptor classes of 12 species of gonodactyloid stomatopods from a variety of photic environments, from intertidal to deep water (> 50 m), to learn how spectral tuning in the different photoreceptor types is modified within different photic environments. Results show that receptors of the peripheral photoreceptors, those outside the midband which are responsible for standard visual tasks such as spatial vision and motion detection, reveal the well-known pattern of decreasing lambdamax with increasing depth. Receptors of midband rows 5 and 6, which are specialized for polarization vision, are similar in all species, having visual lambdamax-values near 500nm, independent of depth. Finally, the spectral receptors of midband rows 1 to 4 are tuned for maximum coverage of the spectrum of irradiance available in the habitat of each species. The quality of the visual worlds experienced by each species we studied must vary considerably, but all appear to exploit the full capabilities offered by their complex visual systems.     

Colour in the eyes of insects

Many insect species have darkly coloured eyes, but distinct colours or patterns are frequently featured. A number of exemplary cases of flies and butterflies are discussed to illustrate our present knowledge of the physical basis of eye colours, their functional background, and the implications for insect colour vision. The screening pigments in the pigment cells commonly determine the eye colour. The red screening pigments of fly eyes and the dorsal eye regions of dragonflies allow stray light to photochemically restore photoconverted visual pigments. A similar role is played by yellow pigment granules inside the photoreceptor cells which function as a light-controlling pupil. Most insect eyes contain black screening pigments which prevent stray light to produce background noise in the photoreceptors. The eyes of tabanid flies are marked by strong metallic colours, due to multilayers in the corneal facet lenses. The corneal multilayers in the gold-green eyes of the deer fly Chrysops relictus reduce the lens transmission in the orange-green, thus narrowing the sensitivity spectrum of photoreceptors having a green absorbing rhodopsin. The tapetum in the eyes of butterflies probably enhances the spectral sensitivity of proximal long-wavelength photoreceptors. Pigment granules lining the rhabdom fine-tune the sensitivity spectra.     

Crumbs regulates polarity and prevents light-induced degeneration of the simple eyes of Drosophila, the ocelli

The evolutionary conserved transmembrane protein Crumbs (Crb) regulates morphogenesis of photoreceptor cells in the compound eye of Drosophila and prevents light-dependent retinal degeneration. Here we examine the role of Crb in the ocelli, the simple eyes of Drosophila. We show that Crb is expressed in ocellar photoreceptor cells, where it defines a stalk membrane apical to the adherens junctions, similar as in photoreceptor cells of the compound eyes. Loss of function of crb disrupts polarity of ocellar photoreceptor cells, and results in mislocalisation of adherens junction proteins. This phenotype is more severe than that observed in mutant photoreceptor cells of the compound eye, and resembles more that of embryonic epithelia lacking crb. Similar as in compound eyes, crb protects ocellar photoreceptors from light induced degeneration, a function that depends on the extracellular portion of the Crb protein. Our data demonstrate that the function of crb in photoreceptor development and homeostasis is conserved in compound eyes and ocelli and underscores the evolutionarily relationship between these visual sense organs of Drosophila. The data will be discussed with respect to the difference in apico-basal organisation of these two cell types.