The eyes of trilobites: The oldest preserved visual system

The oldest preserved visual systems are to be found in the extinct trilobites, marine euarthropods which existed between about 520 and 250 million years ago. Because they possessed a calcified cuticle, they have a good fossil record, and commonly the lens-bearing surfaces of their paired compound eyes are well preserved. The sublensar structures, however, remain unknown. Three kinds of eyes have been distinguished. Holochroal eyes, apomorphic for trilobites, typically have many contiguous small lenses, set on a kidney-shaped visual surface. Lens optics, angular range of vision, and ontogeny have been established for many compound eyes. Some pelagic trilobites have enormous eyes, subtending a panoramic field of view. Schizochroal eyes are found only in one group, the phacopids (Ordovician to Devonian). These have large lenses, separated from each other by cuticular material, and the lenses have a complex doublet or triplet internal structure, which could focus light sharply. The optics of phacopid eyes are becoming increasingly well known despite the fact that there are no direct counterparts in any living arthropods today. Schizochroal eyes are apomorphic for phacopids and were derived by paedomorphosis from a holochroal precursor. Abathochroal eyes are confined to a short-lived Cambrian group, the eodiscids (of which most representatives were blind). Less is known about them than other trilobite eyes and their origins remain obscure. Some trilobite groups had no eyes, but had other kinds of sensory organs. In Upper Devonian times several groups of trilobites independently underwent progressive eye-reduction leading to blindness, related to prevailing environmental conditions of the time. The last trilobites (of Carboniferous and Permian age), however, had normal holochroal eyes, which persisted until the final extinction of trilobites at the end of the Permian.     

Geometric optical optimization of the corneal lens of Notonecta glauca

The optimal shape of the corneal lens of the water bug backswimmer (Notonecta glauca) and the optimal shape and position of the thin transition layer between the distal and proximal units of its cornea are theoretically determined. Using a geometric optical method, first the shape of a geometric interface between the lens units is determined, which eliminates the longitudinal spherical aberration. This interface is investigated for differently formed thick lenses when the medium in contact with the entrance surface of the lens is water or air. The optimal transition layer for the amphibious backswimmer is that, the boundaries of which are the theoretical interfaces for water and air, and the refractive index varies continuously in it. The optimal shape of the corneal lens is determined, with the disadvantageous lenses, with respect to the possible minimal spherical aberration and amount of reflected light from the transition layer, being rejected. The optimal position of the transition layer in the cornea can be obtained from the minimization of the amount of diffracted light on the marginal connection of the layers. The optimal corneal lens for backswimmer has ellipsoid boundary surfaces; the optimal transition layer in it is thin bell-shaped, at the marginal connection of which there is no dimple, the maximum of the layer is on the margin of the cornea. The shape of the theoretically optimal corneal lens, the shape and position of the theoretically optimal transition layer agree well with those of Notonecta glauca. The question posed, the geometric optical method used and the results presented are of general importance, and not only with respect to vision in the bug Notonecta, but also in the fossil trilobites, or in the wave guide theories which have been employed in similar modelling problems, in design of system of lenses without spherical aberration, for example.     

Exceptionally well‐preserved isolated eyes from Cambrian ‘Orsten’ fossil assemblages of Sweden

Abstract: Eyes other than those of trilobites are rarely preserved in the fossil record. We describe here a set of six tiny, isolated, three‐dimensionally preserved compound eyes. These secondarily phosphatized eyes were etched from ‘Orsten’ limestone nodules dated to the Agnostus pisiformis Biozone from the Cambrian Alum Shale Formation of Sweden. The ovoid eyes arise from an elongated stalk, their surface being covered by a mosaic of regular and hexagonal‐shaped facets representing the surface of ommatidia. Facet size and pattern change within the same specimen from the posterior to the anterior end. With regard to some morphological criteria, we grouped the material in two different morphotypes, type A and B, the first being represented by specimens of two different developmental stages. From stage to stage, mostly growth in overall size and addition of new ommatidia was noticed. Among the meiobenthic ‘Orsten’ arthropods, only the crustacean Henningsmoenicaris scutula has been described as possessing stalked eyes, but the eyes of the largest specimen with preserved eyes of this species are much smaller than the new eyes and do not display any kind of ommatidia on their visual surface. However, fragments of larger specimens of H. scutula and the co‐occurrence of this species with the new isolated eyes in the sieving residues make it likely that the latter belong to this species but belong to more advanced stages than those described previously of H. scutula. Ontogenetically, the eye stalks of this fossil crustacean elongate progressively, while the regular hexagonal facets, lacking in early stages, appear later on.     

Microstructure and growth of the lenses of schizochroal trilobite eyes

Lenses within the schizochroal eyes of phacopine trilobites are made principally of calcite, and characterization of them using light microscopy and high‐resolution electron imaging and diffraction has revealed an array of microstructural arrangements that suggest a common original pattern across the suborder. The low convexity lenses of Odontochile hausmanni and Dalmanites sp. contain calcite fibres termed trabeculae. The c axis of trabecular calcite lies parallel to the lens axis, and adjacent trabeculae are distinguished by small differences in their a axis orientations. Despite the common alignment, the boundaries between trabeculae cross‐cut the c axis as they fan out towards the lens base. Trabeculae are absent from the lens immediately beneath the visual surface, and instead, a radial fringe is present and is composed of micrometre‐thick sheets of calcite whose c axes are oriented at a low angle to the visual surface. High convexity lenses are more common than those of lower convexity among the species studied, and they have a much thicker radial fringe. Beneath this fringe, all of the lens calcite is oriented with its c axis parallel to the lens axis and it lacks trabeculae. We propose that both the high and low convexity lenses formed by rapid growth of calcite from a surface that migrated inwards from the cornea, and they may have had an amorphous calcium carbonate precursor. The trabeculae and radial fringes are unlikely to have had any beneficial effect on the transmission or focusing of light, but rather are the outcomes of an elegant solution to the problem of how to construct a biconvex lens from a crystalline solid.     

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.     

Hypostoma of agnostid trilobites

The hypostoma, which is a ventral sclerite that covers the oral region, has recently been discovered in four species of agnostid trilobites. The discovery is significant because the suborder Agnostina is the only major trilobite taxon for which the hypostoma has not been described. The agnostid hypostoma is distinctly different in shape from that of non-agnostid trilobites. Minus its wings, it is widest posteriorly, lacks border furrows, has unusually long wings, and in some species is fenestrate. It is unattached to other sclerites, and presumably was held in place beneath the anterior part of the glabella by muscle tissue. Hypostomal differences probably indicate basic differences in food or feeding habits of agnostid and non-agnostid trilobites. This, along with other evidence, suggests a major divergence in mode of life of these two trilobite groups, and should be given strong consideration in future attempts at trilobite classification.     

The function of the glabellar 'tubercle' in Nileus and other trilobites

The glabellar 'tubercle' of Nileus armadillo (Dalman) is an inverted funnel-shaped thinning in the cuticle, covered by the outer cuticular layer. Its structure is consistent with a function as a light-sensitive organ, whose angular range of light receptivity complements that of the lateral eyes. Median cephalic tubercles of most other trilobites are unlike that of Nileus and are difforent. in structure and position; henco they are unlikely to have been homologous.     

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.     

Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes

Zooplanktivory is one of the most distinct trophic niches in coral reef fishes, and a number of skull traits are widely recognized as being adaptations for feeding in midwater on small planktonic prey. Previous studies have concluded that zooplanktivores have larger eyes for sharper visual acuity, reduced mouth structures to match small prey sizes, and longer gill rakers to help retain captured prey. We tested these three traditional hypotheses plus two novel adaptive hypotheses in labrids, a clade of very diverse coral reef fishes that show multiple independent evolutionary origins of zooplanktivory. Using phylogenetic comparative methods with a data set from 21 species, we failed to find larger eyes in three independent transitions to zooplanktivory. Instead, an impression of large eyes may be caused by a size reduction of the anterior facial region. However, two zooplanktivores (Clepticus parrae and Halichoeres pictus) possess several features interpreted as adaptations to zooplankton feeding, namely large lens diameters relative to eye axial length, round pupil shape, and long gill rakers. The third zooplanktivore in our analysis, Cirrhilabrus solorensis, lacks all above features. It remains unclear whether Cirrhilabrus shows optical specializations for capturing planktonic prey. Our results support the prediction that increased visual acuity is adaptive for zooplanktivory, but in labrids increases in eye size are apparently not part of the evolutionary response.     

Comments on the eyes of tardigrades

A survey is given on the scarce information on the visual organs (eyes or ocelli) of Tardigrada. Many Eutardigrada and some Arthrotardigrada, namely the Echiniscidae, possess inverse pigment-cup ocelli, which are located in the outer lobe of the brain, and probably are of cerebral origin. Occurrence of such organs in tardigrades, suggested as being eyeless, has never been checked. Depending on the species, response to light (photokinesis) is negative, positive or indifferent, and may change during the ontogeny. The tardigrade eyes of the two eutardigrades examined up to now comprise a single pigment cup cell, one or two microvillous (rhabdomeric) sensory cells and ciliary sensory cell(s). In the eyes of the eutardigrade Milnesium tardigradum the cilia are differentiated in an outer branching segment and an inner (dendritic) segment. Because of the scarcity of information on the tardigrade eyes, their homology with the visual organs of other bilaterians is currently difficult to establish and further comparative studies are needed. Thus, the significance of these eyes for the evolution of arthropod visual systems is unclear yet.     

A Curious Rusophycus (Arthropod Ichnofossil) Assemblage from the Upper Ordovician of Ontario,Canada

The ichnogenus Rusophycus includes a wide range of short bilobate excavations generally attributed to variable feeding behaviors of arthropods, especially trilobites. An unusual Rusophycus assemblage from Upper Ordovician Georgian Bay Formation in Ontario departs radically from previously described examples and presents new challenges for understanding the behavior represented by these traces. This specimen is unique in the arrangement of multiple Rusophycus burrows in a circular, lens-shaped array (as opposed to a linear or random arrangement typical of other Rusophycus assemblages). The size and shape of the individual Rusophycus components are consistent with traces attributed to the coeval trilobite Flexicalymene. Multiple Rusophycus assemblages likely reflect aggregations of trilobites in response to a local concentration of food. The topology of this particular Rusophycus assemblage suggests that the trilobites opportunistically exploited a rich and narrowly restricted food source, perhaps the decaying remains of a buried organism.     

Observations on the fluorescence and function of spiders' eyes

Preliminary observations on spiders' eyes showed that certain eyes fluoresce in ultraviolet light and others do not. The response of these eyes to ultraviolet and visible light has been investigated to discover the relationship, if any, of eye fluorescence with eye function.
In the first part of this paper it is shown that of eight spiders from families with widely differing habits, vision and behaviour, five species reacted to light fluctuations and to differences in brightness of the primary colours blue, green and red. Three species did not respond to lightand only two, S. scenicus and E. falcata , indicated a preference for blue light. It was also found that the visual sensitivity of S. secenicus extended into the ultraviolet. The second part of the paper gives the results of examination in ultraviolet light of the eyes of 40 species from 11 families. Spiders with poor sight and a preference for shade generally showed a strong fluorescence of all eyes. The anterior median and lateral eyes of those species with good sight fluoresced only weakly or not at all, whereas the posterior median and lateral eyes ofthese spiders fluoresced brightly.
Freshly cut frozen sections of the eyes of two selected species, S. scenicus with good sight and C. similis with poor sight, were examined with the fluorescence, phase and polarizing microscopes. The localization of the fluorescence in these eyes is described and a fluorescent substance, common to all the spiders, was found in the lens of the eyes of most species examined.Additional information on the structure of the cornea and lens was also revealed by phase and polarized light microscopy.
The results suggest that spiders' eyes respond to light in different ways and the fluorescent substance present in the lens of the eyes is related to eye function.     

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.     

The frontal eyes of crustaceans

Frontal eyes of crustaceans (previously called nauplius eye and frontal organs) are usually simple eyes that send their axons to a medial brain centre in the anterior margin of the protocerebrum. Investigations of a large number of recent species within all major groups of the Crustacea have disclosed four kinds of frontal eyes correlated with taxonomic groups and named after them as the malacostracan, ostracod-maxillopodan, anostracan, and phyllopodan frontal eyes. The different kinds of eyes have been established using the homology concept coined by Owen [Owen, R., 1843. Lectures on the comparative anatomy and physiology of the invertebrate animals. Longman, Brown, Green, Longmans, London] and the criteria for homology recommended by Remane [Remane, A., 1956. Die Grundlagen des natürlichen Systems, der vergleichenden Anatomie und der Phylogenetik. 2nd ed. Akademische Verlagsgesellschaft, Geest und Portig, Leipzig]. Common descent is not used as a homology criterion. Frontal eyes bear no resemblance to compound eyes and in the absence of compound eyes, as in the ostracod-maxillopodan group, frontal eyes develop into complicated mirror, lens-mirror, and scanning eyes. Developmental studies demonstrate widely different ways to produce frontal eyes in phyllopods and malacostracans. As a result of the studies of recent frontal eyes in crustaceans, it is concluded by extrapolation that in crustacean ancestors four non-homologous frontal eye types evolved that have remained functional in spite of concurrent compound eyes.     

Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria

The role of Pax6 in eye development in insects and vertebrates supports the view that their eyes evolved from simple pigment-cup ocelli present in their last common ancestors (Urbilateria). The cerebral eyes in errant polychaetes represent prototype invertebrate pigment-cup ocelli and thus resemble the presumed ancestral eyes. We have analysed expression of conserved eye specification genes in the early development of larval and adult pigment-cup eyes in Platynereis dumerilii (Polychaeta, Annelida, Lophotrochozoa). Both larval and adult eyes form in close vicinity of the optic anlagen on both sides of the developing brain ganglia. While pax6 is expressed in the larval, but not in the developing, adult eyes, expression of six1/2 from trochophora stages onwards specifically outlines the optic anlagen and thus covers both the developing larval and adult eyes. Using Platynereis rhabdomeric opsin as differentiation marker, we show that the first pair of adult eye photoreceptor cells is detected within bilateral clusters that transitorily express ath, the Platynereis atonal orthologue, thus resembling proneural sensory clusters. Our data indicate that--similar to insects, but different from the vertebrates--polychaete six1/2 expression outlines the entire visual system from early developmental stages onwards and ath-positive clusters generate the first photoreceptor cells to appear. We propose that pax6-, six1/2- and ath-positive larval eyes, as found in today's trochophora, were present already in Urbilateria.     

The lower lens unit in schizochroal trilobite eyes reduces reflectivity: On the possible optical function of the intralensar bowl

It is shown that the lower lens unit (or intralensar bowl) in the corneal doublet lens of schizochroaleyed trilobites decreases reflectivity. The reflectivity of geometric optically equivalent distally and proximally Huygensian (spherically corrected) singlet lenses is calculated and compared with the reflectivity of the aplanatic doublet lens in the trilobite Crozonaspis struvei. The maximum reflectivity reduction by the intralensar bowl in the doublet lens amounts to 10.5% and 3% by comparison with the corresponding distally and proximally Huygensian singlet lenses, respectively. From this it is concluded that one of the possible functions of the intralensar bowl might be reflectivity reduction and transmissivity enhancement.     

Evolution of eyes

Seeing is important for most species and it has been a key selective advantage throughout evolution. Consequently, there is a remarkable diversity among types of eyes. Animals have converged on eight optical solutions for collecting and focusing light; in contrast, all eyes share the same molecular strategy for absorbing photons. Recent studies have identified similarities in the genetic information that is used in the development of eyes, leading to the hypothesis that distinctly different eye types might have had a monophyletic origin. Across many species, there is a remarkable continuity of the developmental genes that participate in the construction of similar--but not necessarily homologous--eyes.     

Panum's phenomenon and the confluence of signals from the two eyes in stereoscopy

The signals from the two eyes must be routed to allow either eye to have access to the processing mechanisms for position, shape, colour, etc.; at the same time, information as to the eye of origin must be retained for the purposes of stereoscopy. The study of this confluence of signals from the two eyes was approached psychophysically by studying induced position and depth changes of adjacent binocular and monocular stimuli in the human fovea. It was demonstrated that a monocular visual stimulus located near a binocular one acquires a depth signal, according to a scheme originally proposed by Panum. The effect is unspecific as regards feature shape and brightness, and falls off with a length constant of about 15 minutes of arc in the fovea. A monocular stimulus also affects the apparent depth of its binocular neighbour in a centre-surround manner; disparity pooling changes to disparity repulsion when features are separated by distances of about 3 minutes of arc in the fovea. The findings led to the development of a scheme of uniocular connectivity to a matrix of depth units. Excitation patterns here would depend on the state of the input lines, the intrinsic neuronal interaction properties, and contextural configuring influences from other parts of the nervous system. Experiments showing the spatial extent of pooling and repulsive interaction within the disparity domain help to characterize the stimulus processing in this neural ensemble.     

家蚕复眼突变系光泽眼（lu）和光泽小眼（ve）的复眼形态观察

家蚕Bombyx mori复眼突变系光泽眼(lustrous, lu）及光泽小眼(varnished eye, ve）都是由单基因控制的隐性突变, 目前为止, 其突变基因及突变机理还未知。为了了解其复眼突变性状内外部形态结构差异, 本研究以家蚕正常品系大造Dazao （Dz）为对照, 利用光学显微镜及扫描电镜对家蚕Dz, lu和ve的成虫复眼和幼虫单眼表面进行观察, 并利用石蜡切片HE染色技术对3个品系复眼内部结构进行观察。结果表明： 突变体lu和ve的复眼表面形态除了典型的富有光泽外, 复眼形状、 大小和小眼形态、 排列及数量上都与正常型明显不同。突变体lu和ve的角膜、 晶锥、 感杆束及色素细胞均发生了异常。lu和ve不仅是复眼表面形态发生了变化, 其内部结构也发生了很大的变化。本研究为lu和ve突变基因的克隆及突变机理的阐明提供了参考信息。