Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata)

We have examined the fine structure of dorsal rim ommatidia in the compound eye of the three odonate species Sympetrum striolatum, Aeshna cyanea and Ischnura elegans. These ommatidia exhibit several specializations: (1) the rhabdoms are very short, (2) there is no rhabdomeric twist, and (3) the rhabdoms contain only two, orthogonally-arranged microvillar orientations. The dorsal rim ommatidia of several other insect species are known to be anatomically specialized in a similar way and to be responsible for polarization vision. We suggest that the dorsal rim area of the odonate compound eye plays a similar role in polarization vision. Since the Odonata are a primitive group of insects, the use of polarized skylight for navigation may have developed early in insect phylogeny.     

Redifferentiation of dedifferentiated human chondrocytes in high-density cultures

The ommatidia in the ventral two-thirds of the compound eye of male Pieris rapae crucivora are not uniform. Each ommatidium contains nine photoreceptor cells. Four cells (R1-4) form the distal two-thirds of the rhabdom, four cells (R5-8) approximately occupy the proximal one-third of the rhabdom, and the ninth cell (R9) takes up a minor basal part of the rhabdom. The R5-8 photoreceptor cells contain clusters of reddish pigment adjacent to the rhabdom. From the position of the pigment clusters, three types of ommatidia can be identified: the trapezoidal (type I), square (type II), and rectangular type (type III). Microspectrophotometry with an epi-illumination microscope has revealed that the reflectance spectra of type I and type III ommatidia peak at 635 nm and those of type II ommatidia peak at 675 nm. The bandwith of the reflectance spectra is 40-50 nm. Type II ommatidia strongly fluoresce under ultra-violet and violet epi-illumination. The three types of ommatidia are randomly distributed. The ommatidial heterogeneity is presumably crucial for color discrimination.     

Regional differences in a nematoceran retina (Insecta,Diptera)

Summary The compound eye of Psychoda cinerea comprises two types of ommatidia, arranged so as to divide the retina into distinct dorsal and ventral regions. The P-type ommatidium, in the ventral part of the eye, differs fundamentally from the other dipteran ommatidia so far described, and is regarded as a primitive ommatidium. The acone dioptric apparatus is the same in both types, with a spherical lens and four Semper cells, the processes of which expand below the rhabdom to form a ring of pigment sacs. Only the distal region of the rhabdom is surrounded by a continuous ring of screening pigment, formed by 2 primary and 12–16 secondary pigment cells. The highly pigmented retinula cells penetrate the basement membrane proximally at about the level of their nuclei; in this region they are separated from the hemolymph by glial elements. The rhabdomeres R1–6 are fused to form a tube. The two types of ommatidia are defined by the arrangement of the retinula cells R7/8: in the T type the central rhabdomeres are one below the other, in the usual tandem position, whereas in the P type only R8 is central, with R7 in the peripheral ring. In the proximal region of the retina, retinula cells with parallel microvilli in neighboring ommatidia are joined in rows by lateral processes from the R8 cells. All the rhabdomeres are short and not twisted, which suggests that the retinula cells are highly sensitive to direction of polarization. The eye can adapt by a number of retinomotor processes. These findings, together with observations of behavior, imply that the psychodids have well-developed visual abilities.     

Blue and double-peaked green receptors depend on ommatidial type in the eye of the Japanese yellow swallowtail Papilio xuthus

The compound eye of the butterfly Papilio xuthus is composed of three spectrally distinct types of ommatidia. We investigated the blue and double-peaked green receptors that are encountered distally in type I and III ommatidia, by means of intracellular recordings, in vivo fluorescence microscopy, and histology. The blue receptors are R1 and/or R2 photoreceptors; they contain the same mRNA encoding the opsin of the blue-absorbing visual pigment. However, here we found that the sensitivity in the UV wavelength region strongly depends on the ommatidial type; the blue receptors in type I ommatidia have a distinctly depressed UV sensitivity, which is attributed to lateral filtering in the fused rhabdom. In the main, fronto-ventral part of the eye, the R3 and R4 photoreceptors of all ommatidia contain the same set of two mRNAs encoding the opsins of green-absorbing visual pigments, PxL1 and PxL2. The spectral sensitivities are double-peaked, but the UV sensitivity of the R3 and R4 photoreceptors in type I ommatidia appears to be reduced, similar to that of the co-localized blue receptors.     

Fine structure of the first optic ganglion (lamina) of the cockroach, Periplaneta americana

The structural organization of the first optic ganglion (lamina) of the cockroach (Periplaneta americana) was investigated by the use of light and electron microscopy. Each compound eye of the cockroach is composed of up to 2000 visual units (ommatidia) of the fused rhabdom type. The ommatidia themselves consist of eight receptor cells which terminate as axons in either the first or second optic ganglion. Three different short visual fibre types end in two separate strata in the lamina, and one long fibre type ends in the second optic ganglion. Monopolar second-order neurons with wide field branching patterns in the middle stratum of the first synaptic region have postsynaptic contacts with short visual fibres. Horizontal fibre elements with branching patterns at different levels of the lamina apparently form three horizontal plexuses with presynaptic and/or postsynaptic connections to first- and secondorder neurons. The lack of well-organized fibre cartridges containing a constant number of first and second order neurons in each fascicle and the presence of only unistratified wide field monopolar cells could represent, as compared to other insect orders, a primitive stage in the development of the first optic ganglion.     

Development of the compound eyes of dragonflies (Odonata). III. Adult compound eyes

The distribution of ommatidial diameters and interommatidial angles, as determined by measuring the angles between the optic axes of adjacent ommatidia, are mapped across the surface of the compound eyes of a variety of species selected for different adult behaviors, developmental histories, and taxonomic positions. The size of the visual fields, prey capture foveas, foveas composed of large dorsal ommatidia, and other specializations in the numbers of ommatidia that view various directions in the visual field are discussed in relation to adult behavior. Advanced species have less resemblance between their larval and adult eyes than primitive species. In contrast to their larvae, adults increase the monocular resolution of each eye at the expense of binocular vision. Most species have foveas which view in approximately the anterior direction, instead of in a region of binocular overlap, and many species have foveal bands which view along the horizon. Some advanced perching species, which approach their prey and other odonates from below, have an additional vertical foveal band that views along a vertical plane from the anterior direction to a more dorsal direction. The most unusual foveal band is seen in active flying species. The large dorsal ommatidia of the migratory Anax junius, which cover approximately one third of the eye surface, view a narrow region of the visual field that extends along a plane from the most lateral direction of one eye to a dorsal direction, and continues without interruption to the most lateral direction of the other eye.     

Evidence for the priming role of the central retinula cell in ommatidium differentiation of Ephestia kuehniella

Summary In the developing compound eye of Ephestia kuehniella, within the advancing front of differentiation, regular cell clusters arise which consist of a central cell and two flanking cells. The central cell is destined to become the basal retinula cell later in development. Its crucial role in ommatidium formation is confirmed by ³H-thymidine labelling. Eye anlagen labelled early in the pupal stage incorporate thymidine within two distinct zones along the front of differentiation. After the ommatidia are completely differentiated, both zones contain labelled nuclei of all cell types which participate in ommatidia formation. Within the posterior zone, however, the basal retinula cells are always unlabelled, whereas in the anterior they show labelled nuclei. From this observation it must be concluded that the basal retinula cell first terminates proliferation (either alone or together with a few other cells) to become differentiated as the central retinula cell. These results agree with those found in Drosophila and indicate that the ordered stepwise addition of cells to a central founder cell is a widespread principle of ommatidia formation in insects.     

The physical and morphological properties of the pigment screen in the compound eye of a shrimp (Crustacea)

Summary The pigment cells of the compound eye of the shrimps (Crangon crangon andC. allmani) were studied by electron microscopy (SEM and TEM) and microspectrophotometry. The compound eyes of these species contain light-absorbing and -reflecting pigments contained in granules, located in 5 different cells. The light absorbing pigment granules (light screen) are situated in (1) the distal pigment cells, (2) the retinular cells, (3) the basal pigment cells. The reflecting pigment granules are located in (4) the distal, and (5) the proximal reflecting pigment cells. Another innominate cell type investing the ommatidia contains vacuoles without pigment content. The innominate cell type, and the basal absorbing pigment cell (3) listed above, have not earlier been reported for a crustacean species. Measurements of the spectral absorption on sliced and squashed ommatidia show that all components of the light screen have an increased absorption in the wavelength regions 400–450 nm and 530–570 nm, probably due to xanthommatin and ommin. The spectral absorbancy of the reflecting pigment cells were not determined. Similar cells in other species are known to contain pteridines.We thank Prof. Dr. Langer, Bochum, Germany, for his kind help. The work was supported by funds from the Karolinska Institutet to Doc. G. Struwe, and grant NFR No. 2760-007 to Doc. R. Elofsson.     

A functional analysis of compound eye evolution

New data on the phylogenetic relationships of various arthropod groups have spurred interesting attempts to reconstruct the evolution of arthropod nervous and visual systems. Some of the relevant new data are cell identities and developmental processes in the nervous and sensory systems, which is particularly useful for reconstructing the evolution of these systems. Here, we focus on the structure of compound eye ommatidia, and make an evolutionary analysis with functional arguments. We investigate possible routes of evolution that can be understood in terms of selection for improved visual function, and arrive at a number of conclusions that are discussed in the light of recent phylogenetic hypotheses. On the basis of ommatidial focusing structures and the arrangement of receptor cells we show that the evolution of compound eyes proceeded largely independently along at least two lineages from very primitive ancestors. A common ancestor of insects and crustaceans is likely to have had ommatidia with focusing crystalline cones, and colour and/or polarization vision. In contrast, the compound eyes in myriapods and chelicerates are likely to date back to ancestors with corneal lenses and probably without the ability to discriminate colour and polarization.     

The fine structure of the limulus optic nerve

Two complete composite photographs of the optic nerve of Limulus, made by electron microscopy, reveal the presence of neurosecretory granules in the large axons of the rudimentary eye neurons. The number of intermediate sized, (3–7 μ), of eccentric cells corresponds with the number of ommatidia as expected, but only their sheath of Schwann cells show an intimate interfolding. Based on the number of fine axons within the nerve each ommatidium has an average of 12–13 retinular cells. The diameter of their fibers is between 0.2 and 3 μ although the majority are between 1 and 1.5 μ. They are aggregated into bundles of six to seven fibers by the sheath cells although some bundles contain only two, others as many as 181 fibers. There is no indication in these studies that retinular cell axons within a bundle are associated with the same, adjacent, or other pattern of ommatidia. The photographs suggest that physiological activity in retinular cell axons might be detected most easily in the smallest bundles because they contain the fewest, but the larger retinular cell axons.     

粘虫蛾复眼背、腹区视杆结构的差异

根据光学和电子显微镜的观察,粘虫蛾复眼背、腹区域的视杆结构具有以下主要差异:1)背方小眼视杆的长度短于腹方小眼视杆的长度。2)在横切面上,背方小眼视杆的中段近似方形。该段间细胞的视小杆为三角形,每个具有平行排列的微绒毛。整个视杆包含两个互相垂直的微绒毛轴。腹方小眼视杆的中段为风扇形。间细胞的视小杆为“V”字形,微绒毛排列不平行。3)背方小眼基细胞的视小杆几乎位于气管反光层远侧,而腹方小眼甚至延伸到气管反光层内。 在背方和腹方小眼视杆的内段,每个间细胞的微绒毛均平行,且排列在基细胞的大形视小杆周围。更深层,在其它细胞的轴突均已相继出现的水平上,基细胞的大形视小杆仍然可见。 最后,对形态上的特点,在功能上可能具有的一些意义也进行了初步讨论。     

Retinal ultrastructure of the dorsal eye region of Pararge aegeria (Linné) (Lepidoptera: Satyridae)

We examined the fine structure of dorsal rim ommatidia of the compound eye of Pararge aegeria (Lepidoptera: Satyridae) and compared them with ommatidia of the large dorsal region described by Riesenberg (1983 Diploma, University of Munich). 1. The ommatidia of the dorsal rim show morphological specializations known to be typical of the perception of polarized light: (a) the dumb-bell-shaped rhabdoms contain linearly aligned rhabdomeres with only 2 orthogonally arranged microvilli orientations. The rhabdoms are composed of the rhabdomeres of 9 receptor cells, 8 of which are radially arranged. The rhabdomeres of receptor cells VI and V5, as well as D2, D4, D6 and D8 are dorsoventrally aligned, whereas the rhabdomeres of the cells H3 and H7 are perpendicular to them. The rhabdomere of the bilobed 9th retinula cell lies basally and is dorsoventrally aligned, where retinula cell VI and V5 are already axonal. (b) There is no rhabdomeric twist, and (c) the rhabdoms are rather short. 2. However, in the ommatidia of the large dorsal region, only 2 retinula cells (H3 and H7) are suitable for perception of polarized light. 3. Lucifer yellow and horse radish peroxidase were used as tracers to visualize the projections of retinula cell axons of the dorsal rim area and the large dorsal region into the optic neuropils (lamina and medulla). Two receptors (VI and V5) from both the dorsal rim area and the large dorsal region, have long visual fibres projecting into the medulla. The 7 remaining retinula cells of both eye regions, including those that meet the structural requirements for detection of polarized light in the large dorsal region, terminate in the lamina (short visual fibres). These results provide a starting point for further studies to reveal the possible neuronal pathways by which polarized light may be processed.     

Morphology of the compound eye of the giant deep-sea isopod Bathynomus giganteus

The structural organization of the compound eye of the largest known isopod, Bathynomus giganteus, is described from four specimens maintained in the laboratory for as long as two months. Living specimens have not previously been available for study. The two triangular compound eyes measure about 18 mm on the dorsal edge and are separated by an interocular distance of 25 mm. They face forward and slightly downward and may have significant overlap in visual fields. Each eye contains about 3,500 ommatidia in animals of body lengths from 22.5 cm to 37.5 cm. The packing of ommatidia is not uniform across the retina, but is nearly hexagonal in the dorsal central region and nearly square in the ventral and lateral periphery. The dioptric elements in each ommatidium consist of a laminar cornea, which is flat externally and convex internally, and a bipartite crystalline cone. Sometimes seven and sometimes eight retinular cells closely appose the proximal tip of the cone and bear the microvilli of the rhabdom. Proximal to the rhabdom the retinular cells form thin pillars near the periphery of the ommatidium, and the central portion along the optic axis at this level is occupied by interstitial cells that contain massive arrays of clear vesicles thought to serve as reflective elements. The arhabdomeral segments of the retinular cells and the interstitial cells rest on a basement membrane. Within each ommatidium the basement membrane has two extensions with cylindrical cores and thin sheets of dense material and collagen-like filaments. These sheets occupy spaces between adjacent interstitial cells up to the level of the rhabdomeral segments of the retinular cells. Arrays of pigment cells with relatively weak light-screening properties separate adjacent ommatidia. Animals were fixed both in light within a week of being brought from depth into daylight, and after 2 months of maintenance in constant darkness following such daylight exposure. In both cases, microvilli of the rhabdom were severely disrupted and the retinular cytoplasm contained numerous multivesicular bodies. Exposure to natural daylight appears to cause irreversible structural damage to the photoreceptors of these animals.     

Structure and phylogenetic interpretation of diplopod eyes (Diplopoda)

Summary The structural organization of the ocelli of several diplopod species has been studied by means of electron microscopy. The results provide evidence that diplopodan ocelli are derived from typical mandibulate ommatidia, which consequently had been present in diplopod ancestors. The recent representatives of the two sister groups, Pselaphognatha and Chilognatha are characterized by two essentially different types of eye morphology: The eyes of the Pselaphognatha comprise a bilayered rhabdom (built up by 3+4 retinular cells), a few corneagenous cells, a corneal lens, and two vitreous bodies. The latter probably represent relics of a former crystalline cone. On the contrary, the ocelli of the Chilognatha consist of a multilayered rhabdom (built up by a large number of retinular cells), numerous corneagenous cells, and a corneal lens. The dioptric apparatus lacks a crystalline cone. Further structural elements, the distribution of which varies, are the covering cells and processes of hypodermal cells which contain screening pigments. Whereas the eye of the Pselaphognatha can be traced back to a single ommatidium, the ocellus of the Chilognatha can only be interpreted as a merging product of several associated ommatidia or as the result of multiplication and rearrangement of former ommatidial elements. This concept is substantiated by analogous phenomena which occur within other arthropod groups and thus serve as models for the phylogeny of the diplopodan eyes. The comparison of the morphology and the ecology of palaeozoic and recent diplopods demonstrates that the disintegration of former facetted eyes and the modification of ommatidia were induced by the adaptation to cryptic modes of life.     

The emergence of order in the Drosophila pupal retina

During pupation, long-range order is imposed on the autonomously developing ommatidia which compose the Drosophila eye. To accomplish this, eight additional cell types arise: the primary, secondary, and tertiary pigment cells, and the four cells that form the bristle. These cells form an interweaving lattice between ommatidia. The lattice is refined when excess cells are removed to bring neighboring ommatidia into register. Recent evidence suggests that in larval development, local contacts direct cell fate. The same appears to be true during pupal development: the contacts a cell makes predict the cell type it will become. Cells which contact the anterior or posterior cone cells in an ommatidium invariably become primary pigment cells. Cells which contact primary pigment cells from different ommatidia become secondary and tertiary pigment cells. Bristle development is in several ways distinct from ommatidial development. The four cells of each bristle group appear to be immediate descendents of a single founder cell. During their early differentiation, they do not make stereotyped contacts with surrounding ommatidial cells, but do make particular contacts within the bristle group. And unlike the surrounding ommatidia, differentiation of the bristles radiates from the center of the eye to the edges. As cells are removed during two stages of programmed cell death, the bristles are brought into their final position. When all cells in the lattice have achieved their final position, a second stage of retinal development begins as structures specific to each cell type are produced. This paper follows these various stages of pupal development, and suggests how local cell-cell contacts may produce the cells needed for a functional retina.     

The distribution of polarization sensitivity in the crayfish retinula

In many arthropod eyes the ommatidia contain two classes of retinular cells with orthogonally oriented microvilli. These receptors provide the basis for two-channel polarization vision. In several contexts such as navigation or the detection of polarization contrast, two channels may be insufficient. While solutions to this problem are known (e.g. in insects and stomatopod crustaceans) none have been found in the majority of decapods. To examine this issue further, the polarization sensitivity and the E-vector angle eliciting a maximum response (theta (max)) were measured at over 300 loci on the crayfish retinula. The polarization response ratio (which is proportional to polarization sensitivity) was similar at all locations on the retinula. Around the central pole of the eye, theta (max) was distributed about the vertical and horizontal axes. Along the dorsal rim, the distribution of theta (max) exhibits modes at 0 degrees , 45 degrees and 90 degrees and a small mode at 135 degrees relative to the dorso-ventral axis of the eyestalk (0 degrees ). Smaller numbers of cells (20 to 25%) with theta (max )near the diagonal were also found in anterior and posterior retinula areas. Thus crayfish visual interneurons, which integrate signals from multiple ommatidia may have access to a multi-channel polarization analyzer.     

Evidences that hemoglobin switch in the chick embryo depends on erythroid cell line substitution

Chemical identifications of various hemoglobin types were performed on unfractionated erythroid cells derived from chicken embryos at 5 and 7 days of development and on purified primitive and definitive cells. Proteins were pulse-labelled in primitive erythroid cells at various times of culture to identify those actually synthesized. The data show that primitive cells contain and synthesize only embryonic hemoglobins at all stages of maturation and definitive cells contain adult and minor embryonic hemoglobins, but no major embryonic hemoglobins, not even in trace amounts. These results support a model for hemoglobin switch in the chicken embryo based on cell line substitution.     

The structures of dorsal and ventral regions of a dragonfly retina

Summary The apposition eyes of the corduliid dragonfly Hemicordulia tau are each divided by pigment colour, facet size and facet arrangement into three regions: dorsal, ventral, and a posterior larval strip. Each ommatidium has two primary pigment cells, twenty-five secondary pigment cells, and eight receptor cells, all surrounded by tracheae which probably prevent light passing between ommatidia, and reduce the weight of the eye. Electron microscopy reveals that the receptor cells are of two types: small vestigial cells making virtually no contribution to the rhabdom, and full-size typical cells. The ventral ommatidia have a distal typical cell (oriented either horizontally or vertically), four medial typical cells, two proximal typical cells and one full-length vestigial cell. The dorsal ommatidia have only four full-length typical cells, and one distal and three vestigial full-length cells. The cross-section of dorsal rhabdoms is small and circular distally, but expands to a large three-pointed star medially and proximally. The tiered receptor arrangement in the ventral ommatidia is typical of other Odonata but the dorsal structure has not been fully described in other species. Specialised dorsal eye regions are typical of insects that detect others against the sky.     

The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly,<Emphasis Type="Italic"> Pieris rapae crucivora</Emphasis>

The compound eye of Pieris rapae crucivora contains ventrally three types of histologically distinct ommatidia. An ommatidium contains nine photoreceptors, four of which (R1-4) construct the distal tier of the rhabdom. We determined the sensitivity spectra of the R1-4 distal photoreceptors in each type of ommatidia by intracellular electrophysiology and identified UV, blue, double-peaked blue, green, and a green receptor with depressed sensitivity in the violet. We localized these receptors in each type of ommatidia by injecting dye after the recording. In type I ommatidia the R1 and R2 cells are UV and blue receptors. When R1 is UV sensitive, R2 is always blue sensitive, or vice versa. R3 and R4 in type I are both green receptors. In type II, R1 and R2 are both double-peaked blue receptors and R3 and R4 are both green receptors with depressed sensitivity in the violet. In type III, R1 and R2 are both UV, and R3 and R4 are green receptors. The double-peaked blue, and green receptors with depressed sensitivity in the violet in type II ommatidia have depressed sensitivity at 420 nm, which is probably due to the filtering effect of a fluorescing material present in the type II ommatidia. Spectral heterogeneity of ommatidia seems to be a common design of insect compound eyes.     

Patterning the peripheral retina of the fly: decoding a gradient

The peripheral regions of the fly eye show a number of specializations. First, immediately interior to the circumscribing head capsule and completely encircling the rest of the eye lies a thick band of pigment cells (pigment rim; PR). Second, in the dorsal periphery of the eye directly interior to the PR lie the dorsal rim (DR) ommatidia that are specialized polarized light detectors. The equivalent position in the ventral eye is occupied by standard ommatidia. Third, ommatidia characteristically project mechanosensory hairs above their lenses, but in the most peripheral rows (including the DR) the ommatidia are bald. Wingless secreted from the head capsule appears to organize all these peripheral specializations. Higher Wg levels induce PR, intermediate levels induce DR, and lower levels induce baldness. The predisposition of dorsal cells to generate DR ommatidia appears to be endowed by the exclusive dorsal expression of Iroquois genes.