Carsten Lüter

Ciliary photoreceptors in the cerebral eyes of a protostome larva

BackgroundEyes in bilaterian metazoans have been described as being composed of either ciliary or rhabdomeric photoreceptors. Phylogenetic distribution, as well as distinct morphologies and characteristic deployment of different photopigments (ciliary vs. rhabdomeric opsins) and transduction pathways argue for the co-existence of both of these two photoreceptor types in the last common bilaterian ancestor. Both receptor types exist throughout the Bilateria, but only vertebrates are thought to use ciliary photoreceptors for directional light detection in cerebral eyes, while all other invertebrate bilaterians studied utilize rhabdomeric photoreceptors for this purpose. In protostomes, ciliary photoreceptors that express c-opsin have been described only from a non-visual deep-brain photoreceptor. Their homology with vertebrate rods and cones of the human eye has been hypothesized to represent a unique functional transition from non-visual to visual roles in the vertebrate lineage.ResultsTo test the hypothesis that protostome cerebral eyes employ exclusively rhabdomeric photoreceptors, we investigated the ultrastructure of the larval eyes in the brachiopod Terebratalia transversa. We show that these pigment-cup eyes consist of a lens cell and a shading pigment cell, both of which are putative photoreceptors, deploying a modified, enlarged cilium for light perception, and have axonal connections to the larval brain. Our investigation of the gene expression patterns of c-opsin, Pax6 and otx in these eyes confirms that the larval eye spots of brachiopods are cerebral eyes that deploy ciliary type photoreceptors for directional light detection. Interestingly, c-opsin is also expressed during early embryogenesis in all potential apical neural cells, becoming restricted to the anterior neuroectoderm, before expression is initiated in the photoreceptor cells of the eyes. Coincident with the expression of c-opsin in the presumptive neuroectoderm, we found that middle gastrula stage embryos display a positive photoresponse behavior, in the absence of a discrete shading pigment or axonal connections between cells.ConclusionsOur results indicate that the dichotomy in the deployment of ciliary and rhabdomeric photoreceptors for directional light detection is not as clear-cut as previously thought. Analyses of brachiopod larval eyes demonstrate that the utilization of c-opsin expressing ciliary photoreceptors in cerebral eyes is not limited to vertebrates. The presence of ciliary photoreceptor-based eyes in protostomes suggests that the transition between non-visual and visual functions of photoreceptors has been more evolutionarily labile than previously recognized, and that co-option of ciliary and rhabdomeric photoreceptor cell types for directional light detection has occurred multiple times during animal evolution. In addition, positive photoresponse behavior in gastrula stage embryos suggests that a discrete shading pigment is not requisite for directional photoreception in metazoans. Scanning photoreception of light intensities mediating cell-autonomous changes of ciliary movement may represent an ancient mechanism for regulating locomotory behavior, and is likely to have existed prior to the evolution of eye-mediated directional light detection employing axonal connections to effector cells and a discreet shading pigment.

Calcite morphology, texture and hardness in the distinct layers of rhynchonelliform brachiopod shells

We have investigated the texture and shell microstructure together with the individual hardness distribution patterns of recent calcitic brachiopods of the species Kakanuiella chathamensis, Liothyrella uva and Liothyrella neozelanica. One of the most distinctive features of the studied species is the number of layers that compose the shell. Kakanuiella chathamensis is built entirely of nano- to microcrystalline primary layer calcite. Liothyrella uva contains a nanocrystalline outer primary layer and an inner fibrous secondary layer. Liothyrella neozelanica is composed of three layers, a nanocrystalline outer primary layer, a columnar secondary and an innermost fibrous tertiary shell layer. Even though Kakanuiella chathamensis consists only of primary layer material we observe some textural features and a pattern in the distribution of hardness within the shell. The texture of Liothyrella uva and of Liothyrella neozelanica is significantly more defined than that of Kakanuiella chathamensis. Within the valves calcite crystal c-axes are perpendicular to and rotate accordingly with the shell vault. In contrast to the valves, a multimodal c-axis distribution pattern is present within the hinge region. The hardness distribution in Liothyrella neozelanica and Liothyrella uva is such that the outermost part of the shell is hard while the innermost shell portion is soft. In general, Liothyrella uva is significantly harder than Liothyrella neozelanica and Kakanuiella chathamensis, even though Kakanuiella chathamensis contains only primary layer calcite.

A new thecideid genus and species (Brachiopoda, Recent) from submarine caves of Osprey Reef (Queensland Plateau, Coral Sea, Australia)

A new thecideid brachiopod genus, Ospreyella Lüter and Wörheide gen. n., with the type species Ospreyella depressa Lüter sp. n., is described from Osprey Reef, Coral Sea, Australia. The morphology of the inner sculpture of the dorsal valve and the manner of larval brooding in a single, ventrally situated brood pouch shows that Ospreyella belongs to the family Lacazellinae within thecideid brachiopods. It is the first member of this family described from the Pacific Ocean. Similarities to the related genera Lacazella and Pajaudina as well as differences to the genus Thecidellina are discussed.

The Magellania venosa biomineralizing proteome: a window into brachiopod shell evolution.

Brachiopods are a lineage of invertebrates well known for the breadth and depth of their fossil record. Although the quality of this fossil record attracts the attention of paleontologists, geochemists, and paleoclimatologists, modern day brachiopods are also of interest to evolutionary biologists due to their potential to address a variety of questions ranging from developmental biology to biomineralization. The brachiopod shell is a composite material primarily composed of either calcite or calcium phosphate in close association with proteins and polysaccharides which give these composite structures their material properties. The information content of these biomolecules, sequestered within the shell during its construction, has the potential to inform hypotheses focused on describing how brachiopod shell formation evolved. Here, using high throughput proteomic approaches and next generation sequencing, we have surveyed and characterized the first shell-proteome and shell-forming transcriptome of any brachiopod, the South American Magellania venosa (Rhynchonelliformea: Terebratulida). We find that the seven most abundant proteins present in the shell are unique to M. venosa, but that these proteins display biochemical features found in other metazoan biomineralization proteins. We can also detect some M. venosa proteins that display significant sequence similarity to other metazoan biomineralization proteins, suggesting that some elements of the brachiopod shell-forming proteome are deeply evolutionarily conserved. We also employed a variety of preparation methods to isolate shell proteins and find that in comparison to the shells of other spiralian invertebrates (such as mollusks) the shell ultrastructure of M. venosa may explain the effects these preparation strategies have on our results.

The first Recent species of the unusual brachiopod Kakanuiella (Thecideidae) from New Zealand deep waters

Abstract A new thecideid brachiopod species Kakanuiella chathamensis sp. nov. is described from deep waters on the Chatham Rise, east of South Island, New Zealand. The new species bears an unusual character combination in the shell morphology of its dorsal valve, displaying a mixture of diagnostic characters of both Recent thecideid subfamilies Thecidellininae and Lacazellinae. The resultant consequences for the systematic position of the genus Kakanuiella are discussed.Abstract A new thecideid brachiopod species Kakanuiella chathamensis sp. nov. is described from deep waters on the Chatham Rise, east of South Island, New Zealand. The new species bears an unusual character combination in the shell morphology of its dorsal valve, displaying a mixture of diagnostic characters of both Recent thecideid subfamilies Thecidellininae and Lacazellinae. The resultant consequences for the systematic position of the genus Kakanuiella are discussed.

Shell development, growth and sexual dimorphism in the Recent thecideide brachiopod Thecidellina meyeri sp. nov. from the Lesser Antilles, Caribbean

A new thecideide brachiopod species, Thecidellina meyeri, is described from the southern Lesser Antilles (Aruba, Bonaire, Curacao), Caribbean Sea, with unique morphological characters which clearly separate it from all other described species of Thecidellina in the region. A virtually complete series of ontogenetic stages is recorded, providing insight into the plasticity of shell development duringgrowth in thecideide brachiopods and offering a well-defined standard for comparison with fossil material. Study of the soft tissue suggests that T. meyeri is dioecious, which contradicts the idea of Thecidellina to be hermaphroditic. The limited distribution and the unexpectedly high species diversity within the genus Thecidellina in the Caribbean region support the idea of allopatric speciation due to limited dispersal ability.

Cryptic speciation in the Recent thecideide brachiopod Thecidellina in the Atlantic and the Caribbean

Ultrastructural examination of the brachiopod Thecidellina from three different locations in the Caribbean and the Atlantic revealed that at least three cryptic species are present. One is the type species of the genus, Thecidellina barretti , which may only occur in Jamaica. The other two, previously lumped into T. barretti , are new to science, viz T. bahamiensis Luter & Logan sp. nov. from the Bahamas and T. williamsi Luter & Logan sp. nov. from Cape Verde. All three species clearly differ not only in their provenance, but also in specific shell characters, such as spiculation of the ventral valve, presence of a ventral median ridge, shape of two holes in the intrabrachial ridge of the dorsal valve and the structure of the interbrachial lobes. The identification of three instead of a single species and their supposed allopatric speciation is discussed with regard to the thecideide life cycle and independent models of larval dispersal in the Caribbean, based on oceanographic data.

Larval brooding and development of the micromorph rhynchonellid Tethyrhynchia mediterranea (Brachiopoda: Recent)

Two developmental stages of the micromorph rhynchonellid Tethyrhynchia mediterranea (Brachiopoda: Tethyrhychiidae) are described using scanning electron microscopy (SEM). They were found in niches of the mantle cavity of adult females, as T. mediterranea broods its offspring between the protecting valves of the shell. The developmental stages of T. mediterranea are very small (∼120 μm), but relative to adult body size of up to 1·2 mm in length they are larger than any other lecithotrophic brachiopod larva. Dispersal ability and phylogeography of T. mediterranea in the Mediterranean Sea is discussed.

Checklist of Recent thecideoid brachiopods from the Indian Ocean and Red Sea, with a description of a new species of Thecidellina from Europa Island and a re-description of T. blochmanni Dall from Christmas Island.

Compilation of a checklist of Recent thecideoid brachiopods from the Indian Ocean and Red Sea indicates that members of this superfamily are represented by a small number of species. The subfamily Lacazellinae is represented by Ospreyella maldiviana from the Maldive Islands but the presence of Lacazella cannot yet be confirmed in the Indian Ocean as the holotype of Lacazella mauritiana from Mauritius is lost. The subfamily Thecidellininae is represented by Thecidellina blochmanni from Christmas Island in the eastern Indian Ocean and the Red Sea while a new species T. europa is here described from Europa Island in the Mozambique Channel. The subfamily Minutellinae is represented by Minutella minuta from Samper Bank and Walters Bank in the south-western Indian Ocean and in the Red Sea. Since the holotype of Thecidellina blochmanni from Flying Fish Cove, Christmas Island is also lost, this species is re-described and illustrated mainly from topotypes in the Museum für Naturkunde, Berlin, from which a suggested neotype has been selected.

Overcoming the fragility – X-ray computed micro-tomography elucidates brachiopod endoskeletons

IntroductionThe calcareous shells of brachiopods offer a wealth of informative characters for taxonomic and phylogenetic investigations. In particular scanning electron microscopy (SEM) has been used for decades to visualise internal structures of the shell. However, to produce informative SEM data, brachiopod shells need to be opened after chemical removal of the soft tissue. This preparation occasionally damages the shell. Additionally, skeletal elements of taxonomic/systematic interest such as calcareous spicules which are loosely embedded in the lophophore and mantle connective tissue become disintegrated during the preparation process.ResultsUsing a nondestructive micro-computed tomography (μCT) approach, the entire fragile endoskeleton of brachiopods is documented for the first time. New insights on the structure and position of tissue-bound skeletal elements (spicules) are given as add ons to existing descriptions of brachiopod shell anatomy, thereby enhancing the quality and quantity of informative characters needed for both taxonomic and phylogenetic studies. Here, we present five modern, articulated brachiopods (Rectocalathis schemmgregoryi n. gen., n. sp., Eucalathis sp., Gryphus vitreus, Liothyrella neozelanica and Terebratulina retusa) that were X-rayed using a Phoenix Nanotom XS 180 NF. We provide links to download 3D models of these species, and additional five species with spicules can be accessed in the Supplemental Material. In total, 17 brachiopod genera covering all modern articulated subgroups and 2 inarticulated genera were X-rayed for morphological analysis. Rectocalathis schemmgregoryi n. gen., n. sp. is fully described.ConclusionMicro-CT is an excellent non-destructive tool for investigating calcified structures in the exo- and endoskeletons of brachiopods. With high quality images and interactive 3D models, this study provides a comprehensive description of the profound differences in shell anatomy, facilitates the detection of new delicate morphological characters of the endoskeleton and gives new insights into the body plan of modern brachiopods.