Ciliary photoreceptors in the cerebral eyes of a protostome larva

Background: Eyes 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 nonvisual 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. Results: To 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. Conclusions: Our 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

Spatial patterns in the distribution of benthic assemblages across a large depth gradient in the Coral Sea, Australia

The Queensland Plateau in the Coral Sea off north-eastern Australia supports numerous submerged and emergent reefs. Osprey Reef is an emergent reef at the northern tip of the plateau ~1500 m in elevation. Over such a large depth gradient, a wide range of abiotic factors (e.g. light, temperature, substratum etc.) are likely to influence benthic zonation. Despite the importance of understanding the biodiversity of Australia's Coral Sea, there is a lack of biological information on deep-water habitats below diving depths. Here we used a deep-water ROV transect to capture video, still photos and live samples over a depth range spanning 92 to 787 m at North Horn on Osprey Reef. Video analysis, combined with bathymetry data, was used to identify the zones of geomorphology and the benthic assemblages along the depth gradient. There were marked changes in the geomorphology and the substrate along this depth gradient which likely influence the associated benthos. Cluster analysis indicated five benthic assemblage groups, which showed clear zonation patterns and were generally predictable based on the depth and sedimentary environment. These results are the first quantitative observations to such depths and confirm that the waters of the Coral Sea support diverse benthic assemblages, ranging from shallow-water coral reefs to mesophotic coral ecosystems, to deep-water azooxanthellate corals and sponge gardens. The knowledge provided by our study can inform management plans for the Coral Sea Commonwealth Marine Reserve that incorporate the deeper reef habitats and help to minimise future damage to these marine ecosystems

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

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.Peer Reviewe

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, Curaçao), 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 during growth 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.Peer Reviewe

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

This publication is with permission of the rights owner freely accessible due to an Alliance licence and a national licence (funded by the DFG, German Research Foundation) respectively.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.Peer Reviewe

How brachiopods get covered with nanometric silicon chips.

The investigation of an early pelagic juvenile of the discinid brachiopod Discinisca cf. tenuis elucidates the so far enigmatic origin of nanometric silicon chips covering the brachiopod's juvenile shell. The siliceous tablets are products of an intracellular process within specialized cells of the animal's inner mantle epithelium. These specialized cells are arranged in a circumferential row and contain vesicles, which provide 'reaction chambers' osmotically separated from the cytoplasm. Up to 15 tablets per vesicle are released into the cell by vesicle burst, followed by a coordinated extrusion onto the periostracum. In conjunction with the conveyor belt mechanism of periostracum formation, the regime of tablet release accounts for the highly ordered arrangement of siliceous tablets in parts of the shell's surface. The siliceous tablets are discussed as a protective cover against solar radiation, inherited from Palaeozoic linguliform brachiopods

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 Lüter & Logan sp. nov. from the Bahamas and T. williamsi Lüter & 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.Peer Reviewe