Eye evolution at high resolution: The neuron as a unit of homology

Based on differences in morphology, photoreceptor-type usage and lens composition it has been proposed that complex eyes have evolved independently many times. The remarkable observation that different eye types rely on a conserved network of genes (including Pax6/eyeless) for their formation has led to the revised proposal that disparate complex eye types have evolved from a shared and simpler prototype. Did this ancestral eye already contain the neural circuitry required for image processing? And what were the evolutionary events that led to the formation of complex visual systems, such as those found in vertebrates and insects? The recent identification of unexpected cell-type homologies between neurons in the vertebrate and Drosophila visual systems has led to two proposed models for the evolution of complex visual systems from a simple prototype. The first, as an extension of the finding that the neurons of the vertebrate retina share homologies with both insect (rhabdomeric) and vertebrate (ciliary) photoreceptor cell types, suggests that the vertebrate retina is a composite structure, made up of neurons that have evolved from two spatially separate ancestral photoreceptor populations. The second model, based largely on the conserved role for the Vsx homeobox genes in photoreceptor-target neuron development, suggests that the last common ancestor of vertebrates and flies already possessed a relatively sophisticated visual system that contained a mixture of rhabdomeric and ciliary photoreceptors as well as their first- and second-order target neurons. The vertebrate retina and fly visual system would have subsequently evolved by elaborating on this ancestral neural circuit. Here we present evidence for these two cell-type homology-based models and discuss their implications.     

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.     

Developmental genetics: vertebrates and insects see eye to eye

The results of a number of recent studies indicate that eye development in insects and vertebrates may have more features in common than hitherto suspected. The results support the possibility that insect and vertebrate eyes evolved from a complex ancestral organ.     

Fundamental differences in the optical structure of the eyes of nocturnal and diurnal mosquitoes

We have studied the anatomy and optics of the eyes of a range of mosquito species from the wholly dark-active blood-feeding Anopheles gambiae to the diurnal plant-feeder Toxorhynchites brevipalpis. Consistent with studies by Satô in the 1950s, we find that dark-active and crepuscular species have short fused rhabdoms with a conical construction. This maximises the amount of light the rhabdoms receive from the almost hemispherical wide-aperture lenses. Toxorhynchites, on the other hand, has long narrow rhabdomeres that are separated from each other over their entire length, and so resemble the open rhabdoms of advanced flies (Brachycera and Cyclorrhapha). These findings are confirmed by studies of the pseudopupil, whose form indicates the layout of the rhabdomere tips in the focal plane of each ommatidial lens. In anopheline species the pseudopupil is a single undivided ellipse, indicating a fused rhabdom structure, whereas in Toxorhynchites there is a ring of six outer elements surrounding a central one. This means that each rhabdomere views a separate direction in space, and our measurements indicate that, as in higher Diptera, adjacent rhabdomeres share their fields of view with one of the rhabdomeres in the immediately adjacent ommatidia. This in turn means that in the diurnal type of mosquito eye there is a basis for neural superposition, but the fused construction of anopheline rhabdoms precludes this. The Aedes species studied were similar to Anopheles but with lenses of less extreme aperture, and Sabethes cyaneus, a diurnal blood-feeder, was intermediate in structure, with fused conical rhabdoms in the centre of the eye and unfused rhabdomeres around the periphery.     

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.     

The rhabdom structure in the ommatidia of the Heteroptera (Insecta), and its phylogenetic significance

In its plesiomorphic state the insect ommatidium consists of eight retinula cells forming a fused rhabdom. It has long been observed that, in contrast to this pattern, Heteroptera have open rhabdoms. However, there has so far been no comprehensive and comparative study of heteropteran ommatidia. For this reason, we investigated the rhabdom structure in 36 species from all higher groups of Heteroptera, as well as from Coleorrhyncha and Auchenorrhyncha as outgroup representatives. In addition we surveyed the data of earlier authors, which brings the number of examined species to a total of more than 70. All examined Heteroptera do have open rhabdoms, with a system of six peripheral and two central rhabdomeres. Outgroup comparison shows that the open rhabdom is an autapomorphy of the Heteroptera. As for the rhabdom structure within the Heteroptera, we found further autapomorphic patterns in Corixidae (Nepomorpha), Gerromorpha, and Leptopodomorpha. Finally, the Cimicomorpha and Pentatomomorpha share a special pattern of the two central rhabdomeres, which we call V-pattern. This is a new synapomorphy of these two taxa. Accepted: 22 November 1999     

Did neural pooling for night vision lead to the evolution of neural superposition eyes?

Observations of the infrared deep pseudopupil, optical determinations of the corneal nodal point, and histological methods were used to relate the visual fields of individual rhabdomeres to the array of ommatidial optical axes in four insects with open rhabdoms: the tenebrionid beetle Zophobas morio, the earwig Forficula auricularia, the crane fly Tipula pruinosa, and the backswimmer Notonecta glauca.The open rhabdoms of all four species have a central pair of rhabdomeres surrounded by six peripheral rhabdomeres. At night, a distal pigment aperture is fully open and the rhabdom receives light over an angle approximately six times the interommatidial angle. Different rhabdomeres within the same ommatidium do not share the same visual axis, and the visual fields of the peripheral rhabdomeres overlap the optical axes of several near-by ommatidia. During the day, the pigment aperture is considerably smaller, and all rhabdomeres share the same visual field of about two interommatidial angles, or less, depending on the degree of light adaptation. The pigment aperture serves two functions: (1) it allows the circadian rhythm to switch between the night and day sampling patterns, and (2) it works as a light driven pupil during the day.Theoretical considerations suggest that, in the night eye, the peripheral retinula cells are involved in neural pooling in the lamina, with asymmetric pooling fields matching the visual fields of the rhabdomeres. Such a system provides high sensitivity for nocturnal vision, and the open rhabdom has the potential of feeding information into parallel spatial channels with different tradeoffs between resolution and sensitivity. Modification of this operational principle to suit a strictly diurnal life, makes the contractile pigment aperture superfluous, and decreasing angular sensitivities together with decreasing pooling fields lead to a neural superposition eye.Abbreviations DPP deep pseudopupil - LMC large monopolar cell     

Compound eyes of insects and crustaceans: Some examples that show there is still a lot of work left to be done

Similarities and differences between the 2 main kinds of compound eye (apposition and superposition) are briefly explained before several promising topics for research on compound eyes are being introduced. Research on the embryology and molecular control of the development of the insect clear‐zone eye with superposition optics is one of the suggestions, because almost all of the developmental work on insect eyes in the past has focused on eyes with apposition optics. Age‐ and habitat‐related ultrastructural studies of the retinal organization are another suggestion and the deer cad Lipoptena cervi, which has an aerial phase during which it is winged followed by a several months long parasitic phase during which it is wingless, is mentioned as a candidate species. Sexual dimorphism expressing itself in many species as a difference in eye structure and function provides another promising field for compound eye researchers and so is a focus on compound eye miniaturization in very small insects, especially those that are aquatic and belong to species, in which clear‐zone eyes are diagnostic or are tiny insects that are not aquatic, but belong to taxa like the Diptera for instance, in which open rather than closed rhabdoms are the rule. Structures like interommatidial hairs and glands as well as corneal microridges are yet another field that could yield interesting results and in the past has received insufficient consideration. Finally, the dearth of information on distance vision and depth perception is mentioned and a plea is made to examine the photic environment inside the foam shelters of spittle bugs, chrysales of pupae and other structures shielding insects and crustaceans.     

Different retina-lamina projections in mosquitoes with fused and open rhabdoms

Anopheles gambiae and Toxorhynchites brevipalpis represent the nocturnal and diurnal extremes of the mosquito light intensity range, and their eyes are structurally very different. A. gambiae has fused rhabdoms with huge acceptance angles, whereas T. brevipalpis has open rhabdoms with rhabdomere acceptance angles comparable with those of advanced (brachyceran) flies. Here, we show that the retina-lamina projections are consistent with these differences. The short receptor axons from each ommatidium in A. gambiae insert as a group between four lamina monopolar cell clusters. In T. brevipalpis axon bundles from each ommatidium undergo a twist in their passage through the nuclear layer of the lamina, and then fan out into a space the diameter of which is about twice the separation of the monopolar cell clusters. This arrangement is consistent with a neural superposition mechanism closely similar to that found in higher Diptera, but which must have evolved independently.     

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.     

Chordate betagamma-crystallins and the evolutionary developmental biology of the vertebrate lens

Several animal lineages, including the vertebrates, have evolved sophisticated eyes with lenses that refract light to generate an image. The nearest invertebrate relatives of the vertebrates, such as the ascidians (sea squirts) and amphioxus, have only basic light detecting organs, leading to the widely-held view that the vertebrate lens is an innovation that evolved in early vertebrates. From an embryological perspective the lens is different from the rest of the eye, in that the eye is primarily of neural origin while the lens derives from a non-neural ectodermal placode which invaginates into the developing eye. How such an organ could have evolved has attracted much speculation. Recently, however, molecular developmental studies of sea squirts have started to suggest a possible evolutionary origin for the lens. First, studies of the Pax, Six, Eya and other gene families have indicated that sea squirts have areas of non-neural ectoderm homologous to placodes, suggesting an origin for the embryological characteristics of the lens. Second, the evolution and regulation of the betagamma-crystallins has been studied. These form one of the key crystallin gene families responsible for the transparency of the lens, and regulatory conservation between the betagamma-crystallin gene in the sea squirt Ciona intestinalis and the vertebrate visual system has been experimentally demonstrated. These data, together with knowledge of the morphological, physiological and gene expression similarities between the C. intestinalis ocellus and vertebrate retina, have led us to propose a hypothesis for the evolution of the vertebrate lens and integrated vertebrate eye via the co-option and combination of ancient gene regulatory networks; one controlling morphogenetic aspects of lens development and one controlling the expression of a gene family responsible for the biophysical properties of the lens, with the components of the retina having evolved from an ancestral photoreceptive organ derived from the anterior central nervous system.     

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.     

Optical parameters of euphausiid eyes as a function of habitat depth

Summary The relationships between habitat depth, eye diameter relative to body length, and the dimensions of rhabdoms and crystalline cones have been examined for 13 species of three oceanic euphausiid genera with habitats ranging from near-surface waters to the deep-sea. Rate of eye growth decreases with depth. Longer rhabdoms may increase the visual sensitivity to point and extended light sources by an eye of a particular size with depth. Larger interommatidial angles suggest that visual acuity decreases at depth. Depth-related changes in euphausiid eyes are considered with respect to the probable roles of vision and bioluminescence in the deep-sea. Unusual features of the eyes of several species are described.     

Developmental evolution of the insect retina: insights from standardized numbering of homologous photoreceptors

The canonical number of eight photoreceptors and their arrangement in the ommatidia of insect compound eyes is very conserved. However significant variations exist in selective groups, such as the Lepidoptera and Hymenoptera, which independently evolved additional photoreceptors. For this and historical reasons, heterogeneous labeling conventions have been in use for photoreceptor subtypes, despite developmentally and structurally well-defined homologies. Extending earlier efforts, we introduce a universal photoreceptor subtype classification key that relates to the Drosophila numbering system. Its application is demonstrated in major insect orders, with detailed information on the relationship to previous conventions. We then discuss new insights that result from the improved understanding of photoreceptor subtype homologies. This includes evidence of functionally imposed ground rules of differential opsin expression, the underappreciated role of R8 as ancestral color receptor, the causes and consequences of parallel R7 photoreceptor addition in Hymenoptera and Lepidoptera, and the ancestral subfunctionalization of outer photoreceptors cells, which may be only developmentally recapitulated in Drosophila. We conclude with pointing out the need for opsin expression data from a wider range of insect orders.     

Interspecific variations in the morphology and ultrastructure of the rhabdoms of oplophorid shrimps

Interspecific variations in rhabdom structure between various oplophorid shrimps are described and the differences are related to the light environment at different depths within the mesopelagic zone. The ultrastructure of the distal rhabdom in these species is described for the first time. Quantitative measurements show that the proportion of the rhabdom layer occupied by the distal rhabdom varies from 3.5-25% in the dorsoventral plane of the eye of Systellaspis debilis. The distal rhabdom occupies less than 1% of the rhabdoms in the eye of Acanthephyra pelagica, where it can only be seen by using the electron microscope. It is suggested that the rhabdoms of those species that remain within the photic zone (such as S. debilis) are adapted to maximize contrast, whereas in those whose depth ranges extend into the aphotic zone (such as A. pelagica) they are adapted for maximum sensitivity.     

Reconstruction of ancestral FGLamide-type insect allatostatins: a novel approach to the study of allatostatin function and evolution

Allatostatins (ASTs) are a class of regulatory neuropeptides, with diverse functions, found in an array of invertebrate phyla. ASTs have complex gene structure, in which individual ASTs are cleaved from a precursor peptide. Little is known about the molecular evolution of AST structure and function, even in extensively studied groups such as cockroaches. This paper presents the application of a novel technique for the analysis of this system, that of ancestral reconstruction, whereby ancestral amino acid sequences are resurrected in the laboratory. We inferred the ancestral sequences of a well-characterized peptide, AST 7, for the insect ancestor, as well as several cockroach ancestors. Peptides were assayed for in vitro inhibition of JH production in Diploptera punctata and Periplaneta americana. Our results surprisingly, indicate a decrease in potency of the ancestral cockroach AST7 peptide in comparison with more ancient ones such as the ancestral insect peptide, as well as more recently evolved cockroach peptides. We propose that this unexpected decrease in peptide potency at the cockroach ancestor may be related to the concurrent increase in peptide copy number in the lineages leading to cockroaches. This model is consistent with current physiological data, and may be linked to the increased role of ASTs in the regulation of reproductive processes in the cockroaches.     

栖境不同的两种跳甲复眼结构比较

栖息于荫暗隐蔽处的蛇莓跳甲(Altica fragariae)和向阳开阔地的萎陵跳甲(A.Ampelophaga)的复眼外部形态及小眼微细结构有如下相同特征：两复眼均比较小,呈“八”字型排列在头部近背方的两侧;每个小眼含有一个双凸面的角膜锥体、4个森氏细胞和7个小网膜细胞;2个主色素细胞及11-12个附色素细胞围绕在小眼的外缘;小网膜细胞和色素细胞内均有丰富色素颗粒,当光照强度发生变化时,小网膜细胞内的色素颗粒发生位移;在视杆中段横切面上,视杆由7个微绒毛呈平行排列的矩形视小杆组成,其中的6个视小杆互相连成一个近似六边形的框架,将另一个视小杆围在中央。两种跳甲复眼结构的主要差异有：蛇莓跳甲每个复眼大约仅有150个小眼,而萎陵跳甲约有2印个;复眼曲率半径前者只有后者的一半;视杆中段横切面上,视杆占整个小网膜面积的比率两虫分别为37%和25%,蛇莓跳甲高于萎陵跳甲。对以上形态结构特征可能具有的功能意义进行了初步讨论。     

黑翅土白蚁有翅成虫复眼的形态结构

采用组织切片法光镜下观察黑翅土白蚁Odontotermes formosanus(Shiraki)有翅成虫的复眼形态结构及光、暗适应条件下色素颗粒移动的规律。结果如下:(1)头正前方观,复眼外部形态略呈圆形。(2)有翅成虫复眼类型属于并列像眼,每只复眼约由360个小眼组成。(3)每个小眼是由1套屈光器(1个角膜和1个晶锥)、小网膜色素细胞、视杆和基细胞等几部分组成。小网膜色素细胞内均含有丰富的色素颗粒。(4)在光适应条件状态下,屈光器及视杆周围的色素颗粒主要分布在视杆部位的上侧,暗度适应条件状态时则较均匀地分布于视杆两侧上下;性别对色素颗粒分布无明显影响。     

Ultrastructural study of the naupliar eye of the ostracodeVargula graminicola (Crustacea,Ostracoda)

Summary Ostracodes, like other crustaceans, have a simple naupliar eye that is built upon a theme of three eye cups surrounded by a layer of screening pigments. The single naupliar eye of the ostracodeVargula graminicola is situated medially on the dorsal-anterior side of the body and has three fused eye cups, two dorso-lateral and one ventral. Each eye cup has the following components: (1) pigment cells between the eye cups, (2) tapetal cells, (3) retinular cells with (4) microvillar rhabdomeres, and (5) axons extending into the protocerebrum. Typically two retinular cells contribute lateral microvilli to each rhabdom. The two dorso-lateral eye cups have about 40 retinular cells (20 rhabdoms) and the ventral eye cup has about 30 retinular cells (15 rhabdoms). Typical of myodocopid naupliar eyes (as reported from light microscopic studies), no lens cells or cuticular lenses were observed. The presence of tapetal cells identifies theVargula eye as a maxillopod-ostracode type crustacean naupliar eye. It is unlikely that the naupliar eye ofV. graminicola functions in image formation, rather it probably functions in the mediation of simple taxis towards and away from light.