Specialized ommatidia for polarization vision in the compound eye of cockchafers,Melolontha melolontha (Coleoptera,Scarabaeidae)

Summary The superposition eye of the cockchafer, Melolontha melolontha, exhibits the typical features of many nocturnal and crepuscular scarabaeid beetles: the dioptric apparatus of each ommatidium consists of a thick corneal lens with a strong inner convexity attached to a crystalline cone, that is surrounded by two primary and 9–11 secondary pigment cells. The clear zone contains the unpigmented extensions of the secondary pigment cells, which surround the cell bodies of seven retinula (receptor) cells per ommatidium and a retinular tract formed by them. The seven-lobed fused rhabdoms are composed by the rhabdomeres of the receptor cells 1–7. The rhabdoms are optically separated from each other by a tracheal sheath around the retinulae. The orientation of the microvilli diverges in a fan-like fashion within each rhabdomere. The proximally situated retinula cell 8 does not form a rhabdomere. This standard form of ommatidium stands in contrast to another type of ommatidium found in the dorsal rim area of the eye. The dorsal rim ommatidia are characterized by the following anatomical specializations: (1) The corneal lenses are not clear but contain light-scattering, bubble-like inclusions. (2) The rhabdom length is increased approximately by a factor of two. (3) The rhabdoms have unlobed shapes. (4) Within each rhabdomere the microvilli are parallel to each other. The microvilli of receptor 1 are oriented 90° to those of receptors 2–7. (5) The tracheal sheaths around the retinulae are missing. These findings indicate that the photoreceptors of the dorsal rim area are strongly polarization sensitive and have large visual fields. In the dorsal rim ommatidia of other insects, functionally similar anatomical specializations have been found. In these species, the dorsal rim area of the eye was demonstrated to be the eye region that is responsible for the detection of polarized light. We suggest that the dorsal rim area of the cockchafer eye subserves the same function and that the beetles use the polarization pattern of the sky for orientation during their migrations.     

Structural specializations of the cornea and retina at the dorsal rim of the compound eye in hymenopteran insects

Summary Structurally specialized ommatidia at the dorsal rim of the compound eyes of honey bees have been shown to be indispensable for polarized skylight navigation. In this study numerous other hymenopteran genera belonging to various superfamilies are shown to exhibit similar specializations in this part of the eye: (1) The cornea is penetrated by pore canals, which affect the optics of the ommatidia by scattering the light falling into the eye. In Andrena and Ammophila the cornea contains extensive cavities. (2) Each retinula contains 9 long receptor cells as opposed to 8 long ones in the adjacent dorsal area, and the rhabdom area is increased by a factor of up to 2. In all ant species examined there are no corneal but only retinal specializations at the dorsal rim of the eye. They include a specially shaped rhabdom as in Cataglyphis, in which polarization vision has also been demonstrated.     

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.     

Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye

In many insect species, a dorsal rim area (DRA) in the compound eye is adapted to analyze the sky polarization pattern for compass orientation. In the desert locust Schistocerca gregaria, these specializations are particularly striking. The DRA of the locust consists of about 400 ommatidia. The facets have an irregular shape, and pore canals are often present in the corneae. Screening pigment is missing in the region of the dioptric apparatus suggesting large receptive fields. The rhabdoms are shorter, but about four times larger in cross-section than the rhabdoms of ordinary ommatida. Eight retinula cells contribute to the rhabdom. The microvilli of retinula cell 7 and of cells 1, 2, 5, 6, 8 are highly aligned throughout the rhabdom and form two blocks of orthogonal orientation. The microvilli in the minute rhabdomeres of retinula cells 3 and 4, in contrast, show no particular alignment. As in other insect species, microvillar orientations are arranged in a fan-like pattern across the DRA. Photoreceptor axons project to distinct areas in the dorsal lamina and medulla. The morphological specializations in the DRA of the locust eye most likely maximize the polarization sensitivity and suggest that the locust uses this eye region for analysis of the sky polarization pattern.     

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.     

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.     

亲土苔蛾成虫复眼超微结构

【目的】重叠型眼在昆虫复眼演化中起着重要作用。本研究旨在阐明夜出型亲土苔蛾Manulea affineola复眼类型及结构特征,以期填补灯蛾亚科昆虫复眼研究的空白,扩充夜出型昆虫复眼的特征数据,为探讨重叠型眼的变异趋势及复眼演化提供依据。【方法】运用光学和透射电子显微技术观察亲土苔蛾成虫复眼的超微结构。【结果】亲土苔蛾成虫复眼具有一个透明区,由6个次级色素细胞的透明胞质构成。小眼具8个视网膜细胞,其中1个视网膜细胞较短,仅位于小眼基部。在透明区内,7个视网膜细胞聚集成一束,其远端与晶体束末端相接,但并不形成视杆。在透明区下方,这7个视网膜细胞形成一个中心融合的视杆。在复眼背缘区的小眼的视杆具有近似矩形的横截面,而其余小眼的视杆具多分支状截面。【结论】亲土苔蛾成虫复眼属于重叠型眼;复眼背缘区的矩形视杆很可能与昆虫的偏振敏感性有关。     

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.     

Retinal ultrastructure in the dorsal rim and large dorsal area of the eye of Aglais urticae (Lepidoptera)

Summary The ommatidia in the two dorsal rows at the rim of the eye of Aglais urticae differ from all the other ommatidia of the large dorsal area, in rhabdom structure, length, and configuration of the ninth retinula cell. The type of rhabdom in this dorsal rim zone provides the structural prerequisites for the reception of polarized light; functional subdivision of the retina into two parts is indicated.     

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.     

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.     

螺旋粉虱成虫的复眼形态及其内部结构

采用扫描电镜和组织切片法,观察了螺旋粉虱Aleurodicus dispersus Russell成虫复眼的形态及其显微结构。结果表明,螺旋粉虱复眼半球状,呈“∞”形分布于头部两侧,单个复眼约由253个小眼组成;各小眼面微凸,复眼中心区域小眼多为规则的六边形,密集排列似蜂窝状;近背区边缘小眼多为五边形或近圆形,小眼排列疏松,且少量相邻小眼的间距较大。雌、雄复眼小眼面积约为85μm2。单个小眼由角膜、晶体、网膜细胞及其特化产生的视杆和基细胞等几部分组成。晶体有四个晶锥细胞构成,晶体、视杆周围和色素细胞内均含有大量的色素颗粒。螺旋粉虱的复眼属于并置复眼。光、暗条件下,小眼的色素颗粒分布有所不同。光适应条件下,色素颗粒较均匀地分布于视杆上下两侧;暗适应状态下,色素颗粒则主要分布在视杆上侧和晶体下侧。而在相同的明、暗适应条件下,性别对色素颗粒的分布无显著影响。     

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.     

Specialized ommatidia of the polarization-sensitive dorsal rim area in the eye of monarch butterflies have non-functional reflecting tapeta

Many insects exploit sky light polarization for navigation or cruising-course control. The detection of polarized sky light is mediated by the ommatidia of a small specialized part of the compound eye: the dorsal rim area (DRA). We describe the morphology and fine structure of the DRA in monarch butterflies (Danaus plexippus). The DRA consists of approximately 100 ommatidia forming a narrow ribbon along the dorsal eye margin. Each ommatidium contains two types of photoreceptor with mutually orthogonal microvilli orientations occurring in a 2:6 ratio. Within each rhabdomere, the microvilli are well aligned. Rhabdom structure and orientation remain constant at all retinal levels, but the rhabdom profiles, as seen in tangential sections through the DRA, change their orientations in a fan-like fashion from the frontal to the caudal end of the DRA. Whereas these properties (two microvillar orientations per rhabdom, microvillar alignment along rhabdomeres, ommatidial fan array) are typical for insect DRAs in general, we also report and discuss here a novel feature. The ommatidia of monarch butterflies are equipped with reflecting tapeta, which are directly connected to the proximal ends of the rhabdoms. Although tapeta are also present in the DRA, they are separated from the rhabdoms by a space of approximately 55 μm effectively inactivating them. This reduces self-screening effects, keeping polarization sensitivity of all photoreceptors of the DRA ommatidia both high and approximately equal.     

Wingless eliminates ommatidia from the edge of the developing eye through activation of apoptosis

The Drosophila compound eye is formed by selective recruitment of undifferentiated cells into clusters called ommatidia during late larval and early pupal development. Ommatidia at the edge of the eye, which often lack the full complement of photoreceptors and support cells, undergo apoptosis during mid-pupation. We have found that this cell death is triggered by the secreted glycoprotein Wingless, which activates its own expression in peripheral ommatidia via a positive feedback loop. Wingless signaling elevates the expression of the pro-apoptotic factors head involution defective, grim and reaper, which are required for ommatidial elimination. We estimate that approximately 6-8% of the total photoreceptor pool in each eye is removed by this mechanism. In addition, we show that the retinal apoptosis previously reported in apc1 mutants occurs at the same time as the peripheral ommatidial cell death and also depends on head involution defective, grim and reaper. We consider the implications of these findings for eye development and function in Drosophila and other organisms.     

Manifestations of the eyeless-dominant gene in Drosophila melanogaster

A phenogenetic study was carried out of the eyD-mutation in Drosophila melanogaster which reduces the eye and quantitatively affects different regions of the head capsule originating from the eye imaginal disc. It was shown that the change in eye size is connected causally with changes in certain regions of head capsule: increase in chaetae number or duplication in different regions of the head capsule may be due to the degeneration of presumptive ommatidia. It is supposed that the variable response of chaetae number to the decrease in eye size depends on the origin of chaetae and their topography at different stages of the disc development.     

Ellipse mutations in the Drosophila homologue of the EGF receptor affect pattern formation, cell division, and cell death in eye imaginal discs.

Ellipse alleles are mutations of the EGF-receptor homologue that reduce the number of ommatidia in the eye imaginal disc. Cobalt sulfide staining, expression of hairy and scabrous proteins, and mosaic analysis indicated that Elp mutations affect ommatidial precluster formation in the morphogenetic furrow. BrdU incorporation studies suggest that cells diverted from precluster formation instead enter S-phase after the morphogenetic furrow. Genetic studies suggest that the DER has multiple functions during eye development and that several recessive hypomorphic alleles affect another aspect of DER function that is required after precluster formation. Elp mutations show genetic interactions with the neurogenic mutations Notch and Delta. The small number of ommatidia that differentiate in Elp/Elp are separated more than in wildtype and have been studied to investigate what aspects of ommatidium development are intrinsic to the ommatidium itself. It appears that each developing ommatidium cues the determination of photoreceptors, cone cells, and primary pigment cells, but that the secondary and tertiary pigment cells, and the mechanosensory bristles, can form independently. The normal rotation of ommatidia in the dorsal-ventral axis does not require the presence of the ommatidial array. A short-range signal from a nearby ommatidium is important for mitosis. Cells not close to an ommatidium do not go through mitosis and many die.     

Photoreceptor visual fields, ommatidial array, and receptor axon projections in the polarisation-sensitive dorsal rim area of the cricket compound eye

We made intracellular recordings from the photoreceptors of the polarisation-sensitive dorsal rim area of the cricket compound eye combined with dye marking. By measuring visual field sizes and optical axes in different parts of the dorsal rim area, we assessed the optical properties of the ommatidia. Due to the large angular sensitivities (median about 20°) and the high sampling frequency (about 1 per degree), the visual fields overlap extensively, such that a given portion of the sky is viewed simultaneously by a large number of ommatidia. By comparing the dye markings in the retina and in the optic lobe, the axon projections of the retinula cells were examined. Receptors R1, R2, R5 and R6 project to the lamina, whereas R7 projects to the medulla. The microvilli orientation of the two projection types differ by 90° indicating the two analyser channels that give antagonistic input to polarisation-sensitive interneurons. Using the retinal marking pattern as an indicator for the quality of the intracellular recordings, the polarisation sensitivity of the photoreceptors was re-examined. The polarisation sensitivity of recordings from dye-coupled cells was much lower (median: 4.5) than that of recordings in which only one cell was marked (median: 9.8), indicating that artefactual electrical coupling between photoreceptors can significantly deteriorate polarisation sensitivity. The physiological value of polarisation sensitivity in the cricket dorsal rim area is thus typically about 10. Accepted: 4 November 1999     

Microvillar orientation in the photoreceptors of the ant Cataglyphis bicolor

Polarization sensitivity in arthropod photoreceptors is crucially dependent on the arrangement of the microvilli within the rhabdom. Here, we present an electron-microscopical study in which the degree of microvillar alignment and changes in the cross-sectional areas of the rhabdoms along their length were studied in the compound eye of the desert ant, Cataglyphis bicolor. Serial cross-sections through the retina were taken and the orientation of the microvilli was determined in the photoreceptors of individually identified ommatidia. The reconstructions of microvillar alignment were made in the three anatomically and functionally distinct regions of the Cataglyphis compound eye: the dorsal rim area (DRA), the dorsal area (DA), and the ventral area (VA). The following morphological findings are consistent with polarization sensitivities measured previously by intracellular recordings. (1) The microvilli of the DRA photoreceptors are aligned in parallel along the entire length of the cell from the distal tip of the rhabdom down to its proximal end, near the basement membrane. The microvilli of the retinular cells R1 and R5 are always parallel to each other and perfectly perpendicular, with only minor deviation, to the microvillar orientation of the remaining receptor cells. (2) In the DA and VA regions of the eye, the microvillar tufts of the small receptors R1, R3, R5, R7, and R9 change their direction repetitively every 1-4 7m for up to 90°. In contrast, the large receptor cells R2, R4, R6, and R8 maintain their microvillar orientation rigidly. (3) In the DRA ommatidia, the cross-sectional areas of the rhabdomeres do not change along the length of the rhabdom, but substantial changes occur in the DA and VA ommatidia.