Phylogeny of the Myriapoda – Crustacea – Insecta: a new attempt using photoreceptor structure*

According to molecular sequence data Crustacea and not Myriapoda seem to be the sister‐group to Insecta. This makes it necessary to reconsider how the morphology of their eyes fit with these new cladograms. Homology of facetted eye structures in Insecta (Hexapoda in the sense of Ento‐ and Ectognatha) and Crustacea is clearly supported by identical numbers of cells in an ommatidium (two corneageneous or primary pigment cells, four Semper cells which build the crystalline cone and primarily eight retinula cells). These cell numbers are retained even when great functional modification occurs, especially in the region of the dioptric apparatus. There are two different possibilities to explain differences in eye structure in Myriapoda depending on their phylogenetic position in the cladogram of Mandibulata. In the traditional Tracheata cladogram, eyes of Myriapoda must be secondarily modified. This modification can be explained using the different evolutionary pathways of insect facetted eyes to insect larval eyes (stemmata) as an analogous model system. Comparative morphology of larval insect eyes from all holometabolan orders shows that there are several evolutionary pathways which have led to different types of stemmata and that the process always involved the breaking up the compound eye into individual larval ommatidia. Further evolution led on many occasions to so‐called fusion‐stemmata that occur convergently in each holometabolic order and reveals, in part, great structural similarities to the lateral ocelli of myriapods. As myriapodan eyes cannot be regarded as typical mandibulate ommatidia, their structure can be explained as a modified complex eye evolved in a comparable way to the development to the fusion‐stemmata of insect larvae. The facetted eyes of Scutigera (Myriapoda, Chilopoda) must be considered as secondarily reorganized lateral myriapodan stemmata, the so‐called ‘pseudo‐compound eyes’. New is a crystalline cone‐like vitreous body within the dioptric apparatus. In the new cladogram with Crustacea and Insecta as sister‐groups however, the facetted eyes of Scutigera can be interpreted as an old precursor of the Crustacea – Insecta facetted eye with modified ommatidia having a four‐part crystalline cone, etc. as a synapomorphy. Lateral ocelli of all the other Myriapoda are then modified like insect stemmata. The precursor is then the Scutigera‐Ommatidium. In addition further interpretations of evolutionary pathways of myriapodan morphological characters are discussed.     

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 accessory lateral eye of a diplopod, Cylindroiulus truncorum (Silvestri, 1896) (Diplopoda: Julidae)

Using electron microscopy we describe an accessory lateral eye for Cylindroiulus, a diplopod. The accessory eye is situated at the cell body rind of the optic lobes, deep inside the head, and is composed of six R-cells; a dioptric apparatus is absent. Comparison reveals that many arthropods possess accessory lateral eyes in addition to the compound eyes or lateral ocelli. Their homology and distribution among the arthropod main lineages is discussed along with characters that may be useful for reconstructing phylogeny.     

A serological investigation on the phylogenetic relationship of arthropod classes

Serological kinship of some representative species of arthropods belonging to Crustacea, Arachnida, Myriapoda and Insecta has been studied. There ist weak serological correspondence between the myriapods and insects. The same is the case between Crustacea and Arachnida, and no correspondence was seen between Myriapoda and Insecta on one hand and Crustacea and Arachnida on the other. The results are discussed in relation to the different previous views on the origin and evolution of Arthropoda.     

Neurogenesis in the developing visual system of the branchiopod crustacean Triops longicaudatus (LeConte, 1846): corresponding patterns of compound-eye formation in Crustacea and Insecta?

In the discussion on arthropod phylogeny, the structural evolution of compound eyes and optic ganglia in Crustacea and Insecta is an important topic. On the one hand, many morphological features as well as developmental aspects of the visual system in Insecta and Crustacea correspond in so much detail that eye design in these two groups is likely to have a common euarthropodan ancestor. On the other hand, however, some authors advocate a convergent evolution of the crustacean and insect visual system founding their arguments on differences in the arrangement of the visual neuropils and the fibre connections between Malacostraca and Entomostraca (the "entomostracan enigma"). Therefore, information about cellular aspects of visual system formation in entomostracan Crustacea is likely to enliven this debate, but is not yet available. To fill this gap, we examined the proliferation of neuronal stem cells in the developing visual system of the tadpole shrimp Triops longicaudatus (LeConte, 1846) (Entomostraca, Branchiopoda, Phyllopoda, Calmanostraca, Notostraca) by in vivo incorporation of the proliferation marker bromodeoxyuridine and subsequent immunohistochemical detection. Our results indicate that in the developing visual system of T. longicaudatus, three band-shaped zones containing neuronal stem cells are present corresponding to the proliferation zones found in Malacostraca. We therefore conclude that the ontogenetic mechanisms of visual-system formation are evolutionarily conserved (homologous) in Branchiopoda, Malacostraca, and Insecta.     

Opsin evolution and expression in Arthropod compound Eyes and Ocelli: Insights from the cricket Gryllus bimaculatus

ABSTRACT: BACKGROUND: Opsins are key proteins in animal photoreception. Together with a light-sensitive group, the chromophore, they form visual pigments which initiate the visual transduction cascade when photoactivated. The spectral absorption properties of visual pigments are mainly determined by their opsins, and thus opsins are crucial to understand the adaptations of animal eyes. Studies on the phylogeny and expression pattern of opsins have received considerable attention, but our knowledge about insect visual opsins is still limited. Up to now, researchers have focused on holometabolous insects, while general conclusions require sampling from a broader range of taxa. We have therefore investigated visual opsins in the ocelli and compound eyes of the two-spotted cricket Gryllus bimaculatus, a hemimetabolous insect. RESULTS: Phylogenetic analyses place all identified cricket sequences within the three main visual opsin clades of insects. We assign three of these opsins to visual pigments found in the compound eyes with peak absorbances in the green (515 nm), blue (445 nm) and UV (332 nm) spectral range. Their expression pattern divides the retina into distinct regions: (1) the polarization-sensitive dorsal rim area with blue- and UV-opsin, (2) a newly-discovered ventral band of ommatidia with blue- and green-opsin and (3) the remainder of the compound eye with UV- and green-opsin. In addition, we provide evidence for two ocellar photopigments with peak absorbances in the green (511 nm) and UV (350 nm) spectral range, and with opsins that differ from those expressed in the compound eyes. CONCLUSIONS: Our data show that cricket eyes are spectrally more specialized than has previously been assumed, suggesting that similar adaptations in other insect species might have been overlooked. The arrangement of spectral receptor types within some ommatidia of the cricket compound eyes differs from the generally accepted pattern found in holometabolous insect taxa and awaits a functional explanation. From the opsin phylogeny, we conclude that gene duplications, which permitted differential opsin expression in insect ocelli and compound eyes, occurred independently in several insect lineages and are recent compared to the origin of the eyes themselves.     

The Nymphal Eyes of Parabuthus transvaalicus Purcell, 1899 (Buthidae): An Accessory Lateral Eye in a Scorpion

In P. transvaalicus nymphs, 5 pairs of lateral ocelli each composed of a corneal lens, R-cell units forming a latticed rhabdom, arhabdomeric cells and pigment cells are present. In addition, we found a pair of unpigmented accessory sense organs situated ventroposteriorly to the lateral ocelli in prenymphs as well as in first nymphs. They are composed of primary, rhabdomeric sensory cells, and we infer that they represent a second type of lateral eye. They also comprise sensory units, but lenses and screening pigment are lacking. Their position and cellular architecture corresponds well with that of the “rudimentary” lateral eye of the xiphosuran, Limulus. The occurrence of a bipartite lateral visual system in Chelicerata and Arthropoda is discussed.     

Fine structural organization of the lateral ocelli in two species of Scolopendra (Chilopoda: Pleurostigmophora): an evolutionary evaluation

The lateral ocelli of Scolopendra cingulata and Scolopendra oraniensis were examined by electron microscopy. A pigmented ocellar field with four eyes arranged in a rhomboid configuration is present frontolaterally on both sides of the head. Each lateral ocellus is cup-shaped and consists of a deeply set biconvex corneal lens, which is formed by 230–2,240 cornea-secreting epithelial cells. A crystalline cone is not developed. Two kinds of photoreceptive cells are present in the retinula. 561–1,026 cylindrical retinula cells with circumapically developed microvilli form a large distal rhabdom. Arranged in 13–18 horizontal rings, the distal retinula cells display a multilayered appearance. Each cell layer forms an axial ring of maximally 75 rhabdomeres. In addition, 71–127 club-shaped proximal retinula cells make up uni- or bidirectional rhabdomeres, whose microvilli interdigitate. 150–250 sheath cells are located at the periphery of the eye. Radial sheath cell processes encompass the soma of all retinula cells. Outside the eye cup there are several thin layers of external pigment cells, which not only ensheath the ocelli but also underlie the entire ocellar field, causing its darkly pigmented. The cornea-secreting epithelial cells, sheath cells and external pigment cells form a part of the basal matrix extending around the entire eye cup. Scolopendromorph lateral ocelli differ remarkably with respect to the eyes of other chilopods. The dual type retinula in scolopendromorph eyes supports the hypothesis of its homology with scutigeromorph ommatidia. Other features (e.g. cup-shaped profile of the eye, horizontally multilayered distal retinula cells, interdigitating proximal rhabdomeres, lack of a crystalline cone, presence of external pigment and sheath cells enveloping the entire retinula) do not have any equivalents in scutigeromorph ommatidia and would, therefore, not directly support homology. In fact, most of them (except the external pigment cells) might be interpreted as autapomorphies defining the Pleurostigmophora. Certain structures (e.g. sheath cells, interdigitating proximal rhabdomeres, discontinuous layer of cornea-secreting epithelial cells) are similar to those found in some lithobiid ocelli (e.g. Lithobius). The external pigment cells in Scolopendra species, however, must presently be regarded as an autapomorphy of the Scolopendromorpha.     

Pax6 and eye development in Arthropoda

The arthropod compound eye is one of the three main types of eyes observed in the animal kingdom. Comparison of the eyes seen in Insecta, Crustacea, Myriapoda and Chelicerata reveals considerable variation in terms of overall cell number, cell positioning, and photoreceptor rhabdomeres, yet, molecular data suggest there may be unexpected similarities. We review here the role of Pax6 in eye development and evolution and the relationship of Pax6 with other retinal determination genes and signaling pathways. We then discuss how the study of changes in Pax6 primary structure, in the gene networks controlled by Pax6 and in the relationship of Pax6 with signaling pathways may contribute to our insight into the relative role of conserved molecular-genetic mechanisms and emergence of evolutionary novelty in shaping the ommatidial eyes seen in the Arthropoda.     

Evolution of eye development in arthropods: phylogenetic aspects

The architecture of the adult arthropod visual system for many decades has contributed important character sets that are useful for reconstructing the phylogenetic relationships within this group. In the current paper we explore whether aspects of eye development can also contribute new arguments to the discussion of arthropod phylogeny. We review the current knowledge on eye formation in Trilobita, Xiphosura, Myriapoda, Hexapoda, and Crustacea. All euarthropod taxa share the motif of a proliferation zone at the side of the developing eye field that contributes new eye elements. Two major variations of this common motif can be distinguished: 1. The “row by row type” of Trilobita, Xiphosura, and Diplopoda. In this type, the proliferation zone at the side of the eye field generates new single, large elements with a high and variable cell number, which are added to the side of the eye and extend rows of existing eye elements. Cell proliferation, differentiation and ommatidial assembly seem to be separated in time but spatially confined within the precursors of the optic units which grow continuously once they are formed (intercalary growth). 2. The “morphogenetic front type” of eye formation in Crustacea + Hexapoda (Tetraconata). In this type, there is a clear temporal and spatial separation of the formation and differentiation processes. Proliferation and the initial steps of pattern formation take place in linear and parallel mitotic and morphogenetic fronts (the mitotic waves and the morphogenetic furrow/transition zone) and numerous but small new elements with a strictly fixed set of cells are added to the eye field. In Tetraconata, once formed, the individual ommatidia do not grow any more. Scutigeromorph chilopods take an intermediate position between these two major types. We suggest that the “row by row type” as seen in Trilobita, Xiphosura and Diplopoda represents the plesiomorphic developmental mode of eye formation from the euarthropod ground pattern whereas the “morphogenetic front type” is apomorphic for the Tetraconata. Our data are discussed with regard to two competing hypotheses on arthropod phylogeny, the “Tracheata” versus “Tetraconata” concept. The modes of eye development in Myriapoda is more parsimonious to explain in the Tetraconata hypothesis so that our data raise the possibility that myriapod eyes may not be secondarily reconstructed insect eyes as the prevailing hypothesis suggests.     

Diplopod hemocyanin sequence and the phylogenetic position of the Myriapoda

Hemocyanins are copper-containing respiratory proteins of the Arthropoda that have so far been thoroughly investigated only in the Chelicerata and the Crustacea but have remained unstudied until now in the Myriapoda. Here we report the first sequence of a myriapod hemocyanin. The hemocyanin of Spirostreptus sp. (Diplopoda: Spirostreptidae) is composed of two distinct subunits that are arranged in a 6 x 6 native molecule. The cloned hemocyanin subunit cDNA codes of for a polypeptide of 653 amino acids (75.5 kDa) that includes a signal peptide of 18 amino acids. The sequence closely resembles that of the chelicerate hemocyanins. Molecular phylogenetic analyses reject with high statistical confidence the integrity of the Tracheata (i.e., Myriapoda + Insecta) but give conflicting results on the position of the myriapod hemocyanin. While distance matrix and maximum-likelihood methods support a basal position of the Spirostreptus hemocyanin with respect to the other hemocyanins, parsimony analysis suggests a sister group relationship with the chelicerate hemocyanins. The latter topology is also supported by a unique shared deletion of an alpha-helix. A common ancestry of Myriapoda and Chelicerata should be seriously considered.     

Evolution of the central complex in the arthropod brain with respect to the visual system

Modular midline neuropils, termed arcuate body (Chelicerata, Onychophora) or central body (Myriapoda, Crustacea, Insecta), are a prominent feature of the arthropod brain. In insects and crayfish, the central body is connected to a second midline-spanning neuropil, the protocerebral bridge. Both structures are collectively termed central complex. While some investigators have assumed that central and arcuate bodies are homologous, others have questioned this view. Stimulated by recent evidence for a role of the central complex in polarization vision and object recognition, the architectures of midline neuropils and their associations with the visual system were compared across panarthropods. In chelicerates and onychophorans, second-order neuropils subserving the median eyes are associated with the arcuate body. The central complex of decapods and insects, instead, receives indirect input from the lateral (compound) eye visual system, and connections with median eye (ocellar) projections are present. Together with other characters these data are consistent with a common origin of arcuate bodies and central complexes from an ancestral modular midline neuropil but, depending on the choice of characters, the protocerebral bridge or the central body shows closer affinity with the arcuate body. A possible common role of midline neuropils in azimuth-dependent sensory and motor tasks is discussed.     

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.     

Distribution of photoperiodic receptors in the compound eyes of the bean bug, Riptortus clavatus

  The bean bug, Riptortus clavatus shows a long-day photoperiodic response with respect to the control of adult diapause. The location of photoreceptors for photoperiodism was examined in this species by complete or partial removal of photoreceptor organs. Even after one compound eye or both ocelli were removed, the insects were sensitive to photoperiod. After both compound eyes were removed, however, the insects became reproductive regardless of the photoperiod. Therefore, photoreceptors for photoperiodism were not in the ocelli but in the compound eyes. To clarify whether ommatidia in compound eyes have a regional difference in reception of photoperiod, sensitivity to photoperiod was examined after one compound eye and a part of the contralateral one were removed. Only when the central region of compound eyes was removed did the insects lose sensitivity to photoperiod. It is concluded that the ommatidia in the central region of compound eyes play a principal role in the reception of photoperiod. Accepted: 23 September 1996     

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。     

Das Doppelauge vonEntomobrya muscorum Nicolet (Insecta,Collembola)

Zusammenfassung Der bodenlebende CollembolaEntomobrya muscorum hat an jeder Kopfseite ein loses Aggregat von acht Ommatidien, von denen zwei einen deutlich kleineren Linsendurchmesser aufweisen. Die sechs großen Ommatidien werden als Haupt-, die zwei kleinen als Nebenaugen bezeichnet. Beide Ommatidientypen haben verschieden gebaute Rhabdome, so daß der Komplex ein Doppelauge darstellt. Es wird der Bau der Hauptaugen geschildert. Ihr sensibler Teil setzt sich aus acht Retinulazellen zusammen, die ein offenes Rhabdom in zwei Lagen bilden. Eine zentrale sechste Zelle in der distalen Schicht weicht in ihrer Feinstruktur deutlich von den übrigen ab. Die Rhabdome beider Ommatidientypen werden miteinander verglichen, und ihre funktionelle Bedeutung vor allem in Hinblick auf eine mögliche Arbeitsteilung für eine Polarisationswahrnehmung wird erörtert. Es wird kurz die phylogenetische Bedeutung dieser Augen für die Insekten und die Collembolen selbst angeschnitten.

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The double eye ofEntomobrya muscorum nicolet (Insecta, Collembola)

Summary The ground living CollembolaEntomobrya muscorum has on each side of the head eight circular ommatidia in an arrangement characteristic of the species. Of these two have a distinctly smaller lens. The six big ommatidia are called primary eyes, the two small ones accessory eyes. The two types of ommatidia have different rhabdom structures, so justifying the term double eye. The structure of the primary eyes is described. The photosensitive part is constructed of eight retinula cells which form an open rhabdom in two layers. The central sixth cell in the distal layer is quite different from the others. The rhabdoms of both types are compared. The possible function of the accessory eyes in perception of the e-vector is discussed. The phylogenetic significance of these eyes for the Insecta and the Collembola is considered.

     

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.     

The micromorphology of the nauplius eye of the estuarine calanoid copepod, Sulcanus conflictus Nicholls (Crustacea)

The nauplius eye consists of one median and two lateral ocelli, each within a pigment cup. The three pigment cups are made up from two multi-nucleate pigment cells: each cell forming one lateral cup and half of the median cup. The three cups are lined on the insides by tapetal cells which contain layers of reflectile crystals. Each of the ocelli contains six sensory cells which protrude from the rims of the pigment cups and the protruding parts are sheathed by the conjunctiva cells. The whole eye is enveloped by a thin membrane which also sheaths the proximal parts of the five nerve bundles that leave the eye. All the sensory cells of the lateral ocelli are similar and have rhabdomeric microvilli on the terminal end, and contain phaosomes and a multitude of other organelles and cytoplasmic inclusions. The complex median ocellus contains a superior group of three retinular cells, linked by interdigitating processes, and an inferior group consisting of a large central cell enclosed in two cup-shaped peripheral retinular cells. A two-tiered rhabdome arrangement exists, with a rather complex inferior rhabdome set made up of a central rhabdomere and two hemi-annulate rhabdomeres. The cytoplasm of the retinular cells of the median ocellus lack phaosomes but instead contain double-walled tubular elements, possibly formed by the inpushings of microvilli into adjacent cells. The possible functional significance of the unique arrangement seen in the median ocellus is discussed. The retinular cells are of the inverse type. There are no efferent nerve fibres from the brain nor any nervous connection between the lateral and the median ocelli.     

Morphology of Cambrian lobopodian eyes from the Chengjiang Lagerstätte and their evolutionary significance

Visual organs are widely distributed throughout the animal kingdom and exhibit a great diversity of morphologies. Compound eyes consisting of numerous visual units (ommatidia) are the oldest preserved visual systems of arthropods, but their origins are obscure and hypothetical models for their evolution have been difficult to test in the absence of unequivocal fossil evidence. Here we reveal the detailed eye structures of well-preserved Early Cambrian lobopodians Luolishania longicruris and Hallucigenia fortis from the Chengjiang Lagerstätte, China. These animals possess a pair of eyes composed of at least two visual units, interpreted as pigment cups. Contrary to previous suggestions that Cambrian lobopodians possessed ocellus-like eyes comparable to those of extant onychophorans, this multi-component structure is more similar to the lateral eyes of arthropods. Morphological comparison and phylogenetic analyses indicate that these lobopodian eyes may represent an early stage in the evolution of the ancestral visual system of euarthropods.     

Duplicated Pax6 genes in Glomeris marginata (Myriapoda: Diplopoda), an arthropod with simple lateral eyes

Composite (facetted) eyes comprised by several units, termed ommatidia, are an ancestral feature in the arthropods. Some arthropods, however, do not possess composite eyes, obviously by secondary reduction. Reductions on the level of conserved eye developmental genes are one possibility to reduce the visual system. The genes of the Pax6 family have been shown to be key regulators of visual system development in a wide variety of animals. Reduction of Pax6 expression may therefore be expected in a species with reduced eyes. Here I have investigated the myriapod Glomeris marginata that displays very simple eyes. Glomeris, however, possesses two Pax6 genes that, based on their sequence, are similar to Drosophila eyeless (ey) and twin of eyeless (toy), respectively. Both genes are highly expressed in the optic lobes and the ventral nerve cord of developing embryos. Furthermore, homologs of other high-ranking eye developmental genes like hedgehog, decapentaplegic, dachshund, and homothorax are expressed in the optic lobes. This indicates that eye reduction in Glomeris is not realized at the level of the Pax6 genes or other genes on the upper levels of the eye development network. I suggest instead that the simple eyes of Glomeris are the product of changes at a much lower level in the network, probably at the level of genes directly regulating ommatidia development or ommatidia number and arrangement.