Structural organization of xanthine crystals in the median ocellus of a member of the ancestral insect group Archaeognatha.

Biogenic purine crystals function in vision as mirrors, multilayer reflectors and light scatterers. We investigated a light sensory organ in a primarily wingless insect, the jumping bristletail Lepismachilis rozsypali (Archaeognatha), an ancestral group. The visual system of this animal comprises two compound eyes, two lateral ocelli, and a median ocellus, which is located on the front of the head, pointing downwards to the ground surface. We determined that the median ocellus contains crystals of xanthine, and we obtained insights into their function. To date, xanthine biocrystals have only been found in the Archaeognatha. We performed a structural analysis, using reflection light microscopy, cryo-FIB-SEM, microCT and cryo-SEM. The xanthine crystals cover the bottom of a bowl-shaped volume in the median ocellus, in analogy to a tapetum, and reflect photons to light-sensitive receptors that are spread in the volume without apparent order or preferential orientation. We infer that the median ocellus operates as an irregular multifocal reflector, which is not capable of forming images. A possible function of this organ is to improve photon capture, and by so doing assess distances from the ground surface when jumping by determining changes in the intensity and contrast of the incident light.

Morphological plasticity in response to salinity change in the euryhaline diatom Pleurosira laevis (Bacillariophyta).

Pleurosira laevis is a salt-tolerant diatom distributed around the world. The valve of P. laevis has distinct structures called ocelli, which are sharply defined areas with fine, densely packed pores. Two formae of this diatom, P. laevis f. laevis and P. laevis f. polymorpha, are distinguished from each other by their flat or dome-shaped valve faces and degree of elevation of the ocelli, respectively. In this study, we established 4 strains of P. laevis isolated from freshwaters or coastal areas in Japan and the United States, and tracked the formation of newly formed valves with the fluorescent SDV-specific dye PDMPO in culture under several salinity conditions. The result clearly demonstrated the morphological plasticity of the valves, controlled by environmental salinity. The laevis form and polymorpha form valves were produced at salinities of 2 and 7, respectively. The salinity thresholds dictating the morphological plasticity of the valve were consistent in all 4 strains. A similar morphology to the polymorpha form was reproduced in a freshwater medium with the addition of sorbitol, suggesting that osmotic pressure plays a key role in this morphological plasticity. The highly reproducible and easily manipulated change in morphology makes this diatom an ideal model for lab experiments focusing on the molecular and genetic factors involved with valve morphogenesis.

Revised lineage of larval photoreceptor cells in Ciona reveals archetypal collaboration between neural tube and neural crest in sensory organ formation.

The Ciona intestinalis larva has two distinct photoreceptor organs, a conventional pigmented ocellus and a nonpigmented ocellus, that are asymmetrically situated in the brain. The ciliary photoreceptor cells of these ocelli resemble visual cells of the vertebrate retina. Precise elucidation of the lineage of the photoreceptor cells will be key to understanding the developmental mechanisms of these cells as well as the evolutionary relationships between the photoreceptor organs of ascidians and vertebrates. Photoreceptor cells of the pigmented ocellus have been thought to develop from anterior animal (a-lineage) blastomeres, whereas the developmental origin of the nonpigmented ocellus has not been determined. Here, we show that the photoreceptor cells of both ocelli develop from the right anterior vegetal hemisphere: those of the pigmented ocellus from the right A9.14 cell and those of the nonpigmented ocellus from the right A9.16 cell. The pigmented ocellus is formed by a combination of two lineages of cells with distinct embryonic origins: the photoreceptor cells originate from a medial portion of the A-lineage neural plate, while the pigment cell originates from the lateral edge of the a-lineage neural plate. In light of the recently proposed close evolutionary relationship between the ocellus pigment cell of ascidians and the cephalic neural crest of vertebrates, the ascidian ocellus may represent a prototypic contribution of the neural crest to a cranial sensory organ.

Toward a study of gene regulatory constraints to morphological evolution of the Drosophila ocellar region.

The morphology and function of organs depend on coordinated changes in gene expression during development. These changes are controlled by transcription factors, signaling pathways, and their regulatory interactions, which are represented by gene regulatory networks (GRNs). Therefore, the structure of an organ GRN restricts the morphological and functional variations that the organ can experience-its potential morphospace. Therefore, two important questions arise when studying any GRN: what is the predicted available morphospace and what are the regulatory linkages that contribute the most to control morphological variation within this space. Here, we explore these questions by analyzing a small "three-node" GRN model that captures the Hh-driven regulatory interactions controlling a simple visual structure: the ocellar region of Drosophila. Analysis of the model predicts that random variation of model parameters results in a specific non-random distribution of morphological variants. Study of a limited sample of drosophilids and other dipterans finds a correspondence between the predicted phenotypic range and that found in nature. As an alternative to simulations, we apply Bayesian networks methods in order to identify the set of parameters with the largest contribution to morphological variation. Our results predict the potential morphological space of the ocellar complex and identify likely candidate processes to be responsible for ocellar morphological evolution using Bayesian networks. We further discuss the assumptions that the approach we have taken entails and their validity.

Tubulanus tamias sp. nov. (Nemertea: Palaeonemertea) with Two Different Types of Epidermal Eyes.

Based on specimens collected subtidally (∼10 m in depth) in Tomioka Bay, Japan, we describe the palaeonemertean Tubulanus tamias sp. nov., which differs from all its congeners in body coloration. In molecular phylogenetic analyses based on partial sequences of the nuclear 18S and 28S rRNA genes and histone H3, as well as the mitochondrial 16S rRNA and cytochrome c oxidase subunit I genes, among selected palaeonemerteans, T. tamias nested with part of the congeners in Tubulanus, while the genus as currently diagnosed appears to be non-monophyletic. Molecular cloning detected polymorphism in 28S rDNA sequences in a single individual of T. tamias, indicating incomplete concerted evolution of multiple copies. Tubulanus tamias is peculiar among tubulanids in having 9-10 pigment-cup eyes in the epidermis on either side of the head anterior to the cerebral sensory organs, and remarkably there are two types of eyes. The anterior 8-9 pairs of eyes, becoming larger from anterior to posterior, are completely embedded in the epidermis and proximally abutting the basement membrane; each pigment cup contains bundle of up to seven, rod-shaped structure that resemble a rhabdomeric photoreceptor cell. In contrast, the posterior-most pair of eyes, larger than most of the anterior ones, have an optical cavity filled with long cilia and opening to the exterior, thus appearing to have ciliary-type photoreceptor cells. The size and arrangement of the eyes indicate that the posterior-most pair of eyes are the remnant of the larval (or juvenile) eyes.

Ultrastructure of the dorsal ocellus of Bittacus planus larvae (Mecoptera: Bittacidae) with evolutionary significance.

The Bittacidae are unique in holometabolous insects in that their larvae bear a dorsal ocellus on the frons. The fine structure of the dorsal ocellus, however, has not been investigated to date. Here, the ultrastructure of the larval dorsal ocellus was studied in the hangingfly Bittacus planus Cheng, 1949 using light, scanning, and transmission electron microscopy. The dorsal ocellus of the larvae comprises a cornea, corneagenous cells, and retinula cells. The cornea is a laminated structure. A layer of corneagenous cells is located below the cornea. Numerous retinula cells are arranged tightly beneath the corneagenous cells. The retinula cells modify their adjacent membranes into numerous linear microvilli, which form an analogue of the rhabdom among adjacent retinula cells. The results show that the dorsal ocellus of larval Bittacidae is a highly vestigial organ and appears to be degenerating during the postembryonic development. The presence of the vestigial dorsal ocellus is likely to represent an ancestral plesiomorphy of holometabolous insects, providing new evidence for exploring the evolutionary origin of holometabolous larvae.

Onecut Regulates Core Components of the Molecular Machinery for Neurotransmission in Photoreceptor Differentiation.

Photoreceptor cells (PRC) are neurons highly specialized for sensing light stimuli and have considerably diversified during evolution. The genetic mechanisms that underlie photoreceptor differentiation and accompanied the progressive increase in complexity and diversification of this sensory cell type are a matter of great interest in the field. A role of the homeodomain transcription factor Onecut (Oc) in photoreceptor cell formation is proposed throughout multicellular organisms. However, knowledge of the identity of the Oc downstream-acting factors that mediate specific tasks in the differentiation of the PRC remains limited. Here, we used transgenic perturbation of the Ciona robusta Oc protein to show its requirement for ciliary PRC differentiation. Then, transcriptome profiling between the trans-activation and trans-repression Oc phenotypes identified differentially expressed genes that are enriched in exocytosis, calcium homeostasis, and neurotransmission. Finally, comparison of RNA-Seq datasets in Ciona and mouse identifies a set of Oc downstream genes conserved between tunicates and vertebrates. The transcription factor Oc emerges as a key regulator of neurotransmission in retinal cell types.

Control of size, fate and time by the Hh morphogen in the eyes of flies.

Molecules of the hedgehog (hh) family are involved in the specification and patterning of eyes in vertebrates and invertebrates. These organs, though, are of very different sizes, raising the question of how Hh molecules operate at such different scales. In this paper we discuss the strategies used by Hh to control the development of the two eye types in Drosophila: the large compound eye and the small ocellus. We first describe the distinct ways in which these two eyes develop and the evidence for the key role played by Hh in both; then we consider the potential for variation in the range of action of a "typical" morphogen and measure this range ("characteristic length") for Hh in different organs, including the compound eye and the ocellus. Finally, we describe how different feedback mechanisms are used to extend the Hh range of action to pattern the large and even the small eye. In the ocellus, the basic Hh signaling pathway adds to its dynamics the attenuation of its receptor as cell differentiate. This sole regulatory change can result in the decoding of the Hh gradient by receiving cells as a wave of constant speed. Therefore, in the fly ocellus, the Hh morphogen adds to its spatial patterning role a novel one: patterning along a time axis.

Body size determines eyespot size and presence in coral reef fishes.

Numerous organisms display conspicuous eyespots. These eye-like patterns have been shown to effectively reduce predation by either deflecting strikes away from nonvital organs or by intimidating potential predators. While investigated extensively in terrestrial systems, determining what factors shape eyespot form in colorful coral reef fishes remains less well known. Using a broadscale approach we ask: How does the size of the eyespot relate to the actual eye, and at what size during ontogeny are eyespots acquired or lost? We utilized publicly available images to generate a dataset of 167 eyespot-bearing reef fish species. We measured multiple features relating to the size of the fish, its eye, and the size of its eyespot. In reef fishes, the area of the eyespot closely matches that of the real eye; however, the eyespots "pupil" is nearly four times larger than the real pupil. Eyespots appear at about 20 mm standard length. However, there is a marked decrease in the presence of eyespots in fishes above 48 mm standard length; a size which is tightly correlated with significant decreases in documented mortality rates. Above 75-85 mm, the cost of eyespots appears to outweigh their benefit. Our results identify a "size window" for eyespots in coral reef fishes, which suggests that eyespot use is strictly body size-dependent within this group.

Photoreceptor projection from a four-tiered retina to four distinct regions of the first optic ganglion in a jumping spider.

Jumping spiders have four pairs of eyes (ocelli) of which only the principal eyes (PEs) are used to detect features of objects. Photoreceptors in the retina of the PEs form four layers (PL1-4) and terminate in the first optic ganglion (FOG). Here, we focus on Hasarius adansoni because it has unique depth vision besides color vision and its FOG appears to contribute to the initial processing of these visual modalities. We first investigated the neuroanatomical organization of the FOG. The three-dimensional structure of the FOG revealed by synapsin immunostaining is horseshoe-shaped and consists of four terminal zones (TZ1-4). Then, we traced single photoreceptors through serial sections and found that green-sensitive receptors of PL1 and 2 terminate in TZ1 and 2, respectively, by keeping retinotopic organization. In contrast to TZ1 and 2, TZ3 receives terminals of ultraviolet-sensitive receptors from lateral regions of both PL3 and 4, while photoreceptors of the medial region of PL3 and 4 terminate in TZ4. We further studied details of photoreceptor terminals and the branching pattern of interneurons in the FOG in Golgi stained preparations. Photoreceptors have long lateral processes in each terminal zone. Some photoreceptors terminating in TZ3 have branches innervating TZ1, indicating that TZ1 receives different spectral information. A type of interneuron connects TZ1 and 2, while others have branches within a single terminal zone or in the entire FOG. These results suggest that TZ1 and 2 contribute to color, shape, and depth vision, while TZ3 and 4 have specific roles for UV vision.

Roisinitermesebogoensis gen. & sp. n., an outstanding drywood termite with snapping soldiers from Cameroon (Isoptera, Kalotermitidae).

Termites have developed a wide array of defensive mechanisms. One of them is the mandibulate soldier caste that crushes or pierces their enemies. However, in several lineages of Termitinae, soldiers have long and slender mandibles that cannot bite but, instead, snap and deliver powerful strikes to their opponents. Here, we use morphological and molecular evidence to describe Roisinitermesebogoensis Scheffrahn, gen. & sp. n. from near Mbalmayo, Cameroon. Soldiers of R.ebogoensis are unique among all other kalotermitid soldiers in that they possess snapping mandibles. The imago of R.ebogoensis is also easily distinguished from all other Kalotermitidae by the lack of ocelli. Our study reveals a new case of parallel evolution of snapping mandibles in termites, a complex apparatus responsible of one of the fastest biological acceleration rates measured to date.

Review of the steatiticus-species group of the cuskeel genus Neobythites (Ophidiidae) from the Indo-Pacific, with description of two new species.

This review was motivated by the recent collection of a specimen of the specious cuskeel genus Neobythites (Ophidiidae) off Myanmar and difficulties to identify it based on the available literature. This specimen has an ocellus consisting of a dark oval spot and a concentric white ring placed on the dorsal fin at mid-body, typical for many Neobythites species. It belongs to a group of single-ocellus bearing species which have no or only one weakly developed, flat preopercular spine which we term here the "steatiticus-species group". Before this study, the steatiticus group consisted of six Indo-Pacific species, N. longipes, N. malhaensis, N. malayanus, N. meteori, N. steatiticus, and N. stefanovi, and the Atlantic N. monocellatus. From 136 specimens representing the six Indo-Pacific steatiticus-group species counts or measurements of 12 meristic, 14 body shape, five ocellus and six otolith characters were obtained and compared, revealing two undescribed species. We describe N. gloriae n. sp. from the Arabian Gulf and inner Gulf of Oman based on nine specimens that had been previously misidentified as N. steatiticus and N. stefanovi. The latter species differ from the new species and from each other in the combination of five characters, head length, orbit length, gill-filament length, ocellus-spot distance, and ocellus-spot size. The second new species described is N. lombokensis n. sp. which consists of a single specimen from off SE Lombok, southern Indonesia. It differs from all other steatiticus-group species in having a larger ocellus spot and in several meristic and morphometric characters. The specimen from off Myanmar, eastern Bay of Bengal, was found to belong to N. steatiticus, providing new information on distribution and colour. Diagnoses, updated distribution information, and a key for the eight Indo-Pacific steatiticus-group species are here presented. We discuss our findings with special emphasis on the variation and possible function of colour patterns in Neobythites, being important for understanding the ecology and evolution of this specious genus.

Surprising characteristics of visual systems of invertebrates. / Curiosidades sobre el sistema visual de los invertebrados.

OBJECTIVE: To communicate relevant and striking aspects about the visual system of some close invertebrates. MATERIAL AND METHODS: Review of the related literature. RESULTS: The capacity of snails to regenerate a complete eye, the benefit of the oval shape of the compound eye of many flying insects as a way of stabilising the image during flight, the potential advantages related to the extreme refractive error that characterises the ocelli of many insects, as well as the ability to detect polarised light as a navigation system, are some of the surprising capabilities present in the small invertebrate eyes that are described in this work. CONCLUSIONS: The invertebrate eyes have capabilities and sensorial modalities that are not present in the human eye. The study of the eyes of these animals can help us to improve our understanding of our visual system, and inspire the development of optical devices.

External morphology of eyes and Nebenaugen of caridean decapods-ecological and systematic considerations.

Most caridean decapods have compound eyes of the reflecting superposition kind, and additionally some possess an accessory eye-like organ of unknown function, also referred to as the nebenauge. We examined 308 caridean genera to assess the general morphology of the eye, rostrum length, eye diameter and the presence or absence and, when present, the diameter of the nebenauge. We have attempted to relate these data to ecological and taxonomic considerations. We consider there to be 6 distinct eye types based on the margin between the eyestalk and cornea. The presence of nebenaugen appears to be generally linked to an active lifestyle, as evidenced by the fact that species that have nebenaugen tend to have larger eyes and are more likely to have a distinct rostrum. We suggest that the inconsistencies in its presence/absence under both systematic and ecological lenses may indicate that when present it has various roles relating to behavioural and physiological rhythms.

Ultrastructure of dorsal ocelli of the short-faced scorpionfly Panorpodes kuandianensis (Mecoptera: Panorpodidae).

Dorsal ocelli are important visual organs of insects to perform a variety of behavioral functions. However, the fine structure of ocelli has not been studied in many groups of insects. In this paper the ocellar ultrastructure of the short-faced scorpionfly Panorpodes kuandianensis was investigated using light microscopy and scanning and transmission electron microscopy. The adult of P. kuandianensis possesses one median and two lateral ocelli. Each ocellus comprises a cornea, a layer of corneagenous cells, a clear zone, a retina, and pigment cells. The cornea assumes a domed shape. Under the layer of corneagenous cells is a clear zone, which differs greatly between the median and lateral ocelli, implying they may be divergent in function. The retina comprises elongated retinula cells, which are divided into three regions: a distal rhabdomal region, a middle cytoplasmic region, and a proximal axonal region. In the distal rhabdomal region, most of the rhabdoms are formed by rhabdomeres of two adjacent retinula cells; some are formed by three or four retinula cells. The middle cytoplasmic region comprises the retinula cell segments with nuclei but free of rhabdom. Pigment granules are present among the retinula cells. In the proximal axonal region all retinula cells transform to axons, which synapse with the dendrites of second-order neurons at the base of the ocelli. The relationships among Panorpodidae, Panorpidae and Bittacidae are discussed based on ocellar structure.